Culicidae

Reeves, Will K., Adler, Peter H., Grogan, William L. & Super, Paul E., 2004, Hematophagous and Parasitic Diptera (Insecta) in the Great Smoky Mountains National Park, USA, Zootaxa 483, pp. 1-44 : 12-20

Family Culicidae

Mosquitoes are important vectors of viruses, bacteria, protozoa, and helminths. Some mosquitoes (e.g., Aedes and Ochlerotatus ) are also important pollinators of native plants ( Stoutamire 1968).

The Park had not been surveyed previously for mosquitoes, but 32 species are known from adjacent Knox County ( Hribar & Gerhardt 1986). Species such as Oc. japonicus (Theobald) have recently invaded the USA and could move into the natural rock­pool habitats in the Park ( Peyton et al. 1999; Scott et al. 2001).

Aedes aegypti (Linnaeus)

Collection: North Carolina, Swain Co., Oconaluftee /Ravensford, 4 July 2002, in rain gutter of building.

Aedes aegypti is one of the most important vectors of pathogens to humans worldwide. When temperatures drop below 15°C, Ae. aegypti normally cannot survive ( Christophers 1960). The larva collected from the Park probably represents an accidental reintroduction by a visitor traveling from Florida, Louisiana, or a foreign country. Aedes aegypti has disappeared from most of the USA but it is still present and common in the Florida Keys ( Hribar 2003). Although local transmission of pathogens by Ae. aegypti is unlikely, this species could transmit viruses among Park visitors or serve as a vector of dog heartworm, Dirofilaria immitis (Leidy) . Aedes aegypti is a competent vector of a blood parasite, Shelackia occidentalis Bonorris & Ball , of the fence lizard, Sceloporus undulatus (Green) ( Barnard & Durden 2000) .

Aedes albopictus Skuse

Collections: North Carolina, Swain Co., Oconaluftee /Ravensford, 31 May, 8 and 9 July 2001, biting horse; Twentymile Creek ranger station, 8 July 2001, adult; Tennessee, Cocke Co., Cosby government housing, 3 August 2000, biting humans; Blount Co. Cades Cove, 4 August 2003, pupae from bucket.

Aedes albopictus is an exotic peridomestic species that oviposits in natural and artificial containers. It feeds mostly between dawn and dusk but also bites at night ( Higa et al. 2000). All collections in the Park were made at low elevations around permanent humanbuilt structures. Aedes albopictus colonizes rock holes ( O'Meara et al. 1997), but was not collected in these habitats in the Park. It is a potential vector of disease agents to humans and wildlife in the Park, where it could transmit dog heartworm, West Nile virus, and LaCrosse encephalitis virus. Aedes albopictus could transmit dengue viruses between Park visitors if these pathogens were introduced. Aedes albopictus is a vector of the European onchocercid Dirofilaria repens (Townson) , which infects both domestic dogs and humans ( Cancrini et al. 2003).

Aedes cinereus Meigen

Collections: North Carolina, Swain Co. , Clingman’s Dome sewage treatment plant (1767 meters, 35.5480°N, 83.4924°W), 23 July 2001, larva; Tennessee, Sevier Co., Twin Creeks, 13–27 August 2001, Malaise trap, coll. I. Stocks.

Horsfall (1955) incriminated Ae. cinereus as a vector of tularemia and Dirofilaria sacpiceps Leidy , a filarial nematode of rabbits. Aedes cinereus is the primary bridge vector for Sindbis virus in Europe ( Griffin 2002) and could be an important vector if this virus is introduced into North America. Wright & DeFoliart (1970a) collected blood­engorged females from deer, raccoons, beavers, red foxes, opossums, cottontail rabbits, woodchucks, gray squirrels, fox squirrels, eastern chipmunks, ground squirrels, Peromyscus spp., chickens, woodcocks, and snapping turtles in Wisconsin.

Aedes vexans (Meigen)

Collections: North Carolina, Swain Co., Andrews Bald (1757 meters, 35.5387°N, 83.4943°W), 10–24 May 2001, Malaise trap, coll. Stocks, McCord, Middleton; Oconaluftee/Ravensford, 4 May 2001, CDC light trap; Raven Fork River at Oconaluftee/ Ravensford, 9 June 2001, biting human; Tennessee, Blount Co., Cades Cove, Gum Swamp, 25 April 2001, larvae, coll. M.J. Wetzel & M.A. Morgan; Sevier Co., Clingmans Dome, 24 April–10 May 2001, Malaise trap, (1944 meters, 35.5602°N, 83.4952°W), coll. I. Stocks.

Aedes vexans was one of the most numerous mosquitoes during the spring when it and Oc. canadensis were the predominant human­biting mosquitoes. Of the approximately 300 adults of this species collected at Oconaluftee/Ravensford on 4 May 2001, two were parasitized by a hydryphantid mite, Thyas sp. Wozniak et al. (2001) implicated Ae. vexans as a potential vector of Potosi­like virus in the Carolinas, and Horsfall (1955) noted that Ae. vexans is a laboratory vector for dog heartworm. This mosquito feeds on "reptiles", deer, raccoons, red foxes, opossums, cottontail rabbits, woodchucks, gray squirrels, fox squirrels, eastern chipmunks, ground squirrels, Peromyscus spp., chickens, woodcocks, snapping turtles, and painted turtles ( Wright & DeFoliart 1970a; Barnard & Durden 2000).

Anopheles perplexens Ludlow

Collections: North Carolina, Oconaluftee /Ravensford, 4 May 2001, CDC light trap; Tow String Road (229 meters, 35.5461°N, 83.2995°W), 9 May 2001, dip sample.

Two collections of An. perplexens from the Park represent a range extension for this mosquito. The adult collected at the Oconaluftee/Ravensford site was attracted to ultraviolet light and the larva was collected from a streamside rock hole.

Anopheles punctipennis (Say)

Collections: North Carolina, Haywood Co., Cataloochee , 14 March 2002, biting human, 19 March 2002, biting nose of elk; Purchase Knob, 14 May 2002, well spring, pupae; Swain Co., Oconaluftee/Ravensford, 4 May 2001, CDC light trap, 25 May 2001; Tow String Road, 19 May 2001, roadside seepage; 9 May 2002, biting human; Straight Fork Motor Trail, 19 May 2001, stream overflow pools; 17 June 2001, gravel pool; Lake Fontana (525 meters, 35.4316°N, 83.5955°W), 8 June 2001, pool near dam; Tennessee, Blount Co., Abram’s Creek (336 meters, 35.6105°N, 83.9326°W), no date given, trapped adults, coll. P. Super; Cades Cove, ATBI plot, 26 February to 13 March 2001, Lingren funnel, adult female; Gregorys Cave (610 meters, 35.6098°N, 83.8058°W), 1 October 1999, diapausing adult females; Tremont Institute, 16 July 2001, hand collection, coll. P. Super; Cocke Co., Cosby government housing, 24 March 2000, adults in building; Sevier Co., Goshen Prong (35.5983°N, 83.5675°W), 8–21 May 2001, Malaise trap; Little River at the Sinks (477 meters, 35.6689°N, 83.6621°W), 17 June 2001, rock pool; Myhr Cave, 27 October 1999, diapausing adult females; Roaring Fork Gorge (488 meters, 35.7114°N, 83.4826°W), 16 July 2001, rock pool.

Anopheles punctipennis was the most frequently collected anopheline mosquito in the Park, where it fed on humans. Although it is a competent vector of malaria, local transmission of Plasmodium spp. from infected Park visitors by An. punctipennis is unlikely. Horsfall (1955) indicated that An. punctipennis is a potential vector of dog heartworm. A single engorged female from the nose of a tranquilized elk represents a reestablished host association because elk were recently reintroduced to the Park. Irby & Apperson (1988) collected blood­fed females of An. punctipennis from canids, deer, pigs, and rabbits in eastern North Carolina .

Anopheles quadrimaculatus Say

Collection: North Carolina, Swain Co., Oconaluftee /Ravensford, 4 May 2001, CDC light trap.

A single female of An. quadrimaculatus sensu stricto was trapped at the Oconaluftee/ Ravensford area. Anopheles quadrimaculatus was historically the primary vector of malaria in the southern USA, but is apparently rare in the Park. Therefore, local malaria transmission to Park visitors is unlikely. We found no historical records of malaria in the Park archives. However, the TVA was given authority to control malaria in the Park ( Tennessee Valley Authority 1948). Wozniak et al. (2001) found An. quadrimaculatus sensu lato in South Carolina to be infected with eastern equine encephalomyelitis virus, but no transmission was demonstrated. Anopheles quadrimaculatus feeds on canids and deer more often than on humans in North Carolina ( Irby & Apperson 1988) . It is not a competent vector of avian Plasmodium ( Horsfall 1955) .

Coquillettidia perturbans (Walker)

Collection: Tennessee, Blount Co., Cades Cove, 25 May 2001, at exhaust of soda machine.

A single female of Cq. perturbans was found at dusk hovering near the exhaust vent of a soda vending machine. Coquillettidia perturbans is probably rare in the Park because the larvae require specific host plants that do not grow in most of the Park. Coquillettidia perturbans has been implicated as a potential vector of Potosi and eastern equine encephalomyelitis virus in South Carolina ( Wozniak et al. 2001) .

Culex erraticus (Dyar & Knab)

Collections: North Carolina, Swain Co. Oconaluftee /Ravensford, 4 May 2001, CDC light trap; Tennessee, Cocke Co., Cosby nature trail, 29 May 2001; Blount Co., Gregorys Cave (527 meters, 35.6099°N, 83.8059°W), 1 October 1999, diapausing adults; Sevier Co., Myhr Cave, 27 October 1999, diapausing adults; Goshen Prong (895 meters, 35.6105°N, 83.5424°W), 4–18 June 1999 Malaise trap, coll. Parker, Stocks, & Petersen.

Culex erraticus was the least frequently collected species of Culex in the Park, but adults were occasionally found in caves during the winter. With the introduction of West Nile virus, this species could play a role in the enzootic cycle of the virus. Culex erraticus was found to be infected with eastern equine encephalomyelitis virus in South Carolina ( Wozniak et al. 2001) . Klein et al. (1987) incriminated Cx. erraticus as a vector of Plasmodium floridense Thomspon & Huff to the green anole, Anolis carolinensis (Voigt) .

Culex pipiens Linnaeus

Collections: North Carolina, Haywood Co. Cataloochee , 14 May 2002, ditch; Swain Co., Oconaluftee/Ravensford, 23 May 2001, hand collection, adult male; 31 May 2002, female feeding on pig; Tow String Road, 10 May 2001, roadside ditch; Big Cove Road (195 meters, 35.5078°N, 83.3002°W), 20 June 2001, tractor tires; Smokemont sewage treatment plant, 22 August 2002; Tennessee, Blount Co., Cades Cove, 25 May 2001, females ovipositing in horse watering trough; Sevier Co., Little River at the Sinks, 25 May 2001, rock pools, larvae; Metcalf Bottoms (515 meters, 35.6803°N, 83.6494°W), 17 June 2001, roadside pool; Goshen Prong, 5–12 November 2001, Malaise trap, coll. Parker, Stocks, & Petersen.

Because the genitalia of all reared males matched the description for Cx. pipiens , this species name was used over the ambiguous " Cx. pipiens /quinquefasciatus group.” Culex pipiens is believed to be the most important vector of West Nile virus in the USA ( Nasci et al. 2001). One female from Oconaluftee was infected with the developmental stages of an unidentified filarial nematode. The only biting record in the Park was from hogs, but this mosquito probably feeds on other mammals and birds. Culex pipiens breeds in polluted waters and was the most common mosquito in the Park’s animal water troughs. A single adult from Cataloochee had an unidentified hydryphantid mite attached to its abdomen. Culex pipiens will feed on reptiles and is a vector of protozoan blood parasites, including Saurocytozoon tupinambi Lairson, Shelackia golvani Rogier & Landau, and S. occidentalis ( Barnard & Durden 2000) . Smith et al. (1994) implicated Cx. pipiens as a vector of Hepatozoon sipedon to water snakes ( Nerodia sipedon (Linneaus)) and leopard frogs ( Rana pipiens Schreber ).

Culex restuans Theobald

Collections: North Carolina, Haywood Co., Palmer Chapel (823 meters, 35.6267°N, 83.1096°W), 3 May 2002, dead in window; Cove Creek Gap (1241 meters, 35.632ºN, 83.045ºW), 14 May 2002, in trash; Big Creek (524 meters, 35.7567°N, 83.1048°W), 14 May 2002, mud pool near road; Purchase Knob, 14 May 2002, well spring, pupae; Swain Co. Oconaluftee/Ravensford, 4 May 2001, CDC light trap, 31 May 2001, biting pigs; Clingman’s Dome sewage treatment plant, 22 July 2001, larvae, settling pond; Tow String Road, 15 August 2001, larvae, roadside ditch; swamp at Payne Branch (549 meters, 35.4654°N, 83.8029°W), 16 May 2002, larvae; Tennessee, Cocke Co., Cosby, 14 May 2002, Cosby nature trail mud puddle, larvae; Blount Co., Cades Cove, 4–18 June 2001, Malaise trap, coll. R. Hightower & J. Burbank; Sevier Co., Little River at the Sinks, 25 May 2001, rock holes; Metcalf Bottoms, 17 June 2001, roadside ditch; Goshen Prong, 5– 12 November 2001, Malaise trap, coll. Parker, Stocks, & Petersen; Myhr Cave, 6 January 1999, diapausing adult, coll. K. Langdon.

The natural habitats of Cx. restuans included all elevations in the Park. The larvae from the Clingman’s Dome sewage ponds above 2000 meters elevation potentially represent the highest elevation for mosquito development in the Appalachians. An adult from Cataloochee was infested with an unidentified hydryphantid mite. Culex restuans is a potential vector of West Nile virus and might be involved in the transmission of other arboviruses and pathogens. Culex restuans feeds on reptiles ( Barnard & Durden 2000).

Culex territans Walker

Collections: North Carolina, Haywood Co., Big Creek , 17 August 2001, larvae, rock pool; Cove Creek Gap, 14 May 2002, in trash; Cataloochee, 17 May 2002, larvae, roadside ditch; Purchase Knob, 14 May 2002, larva; Swain Co., Straight Fork Motor Trail, 19 May 2001, stream overflow polls; Tow String Road, 19 May 2001, larvae, rock pools; Oconaluftee/Ravensford, 23 May 2001, larvae; Cherokee, 31 May 2001, larvae, roadside seepage with pool; swamp at Payne Branch, 16 May 2002, larvae; Smokemont, 22 August 2002; Tennessee, Cosby, Cosby nature trail, 14 May 2002, adults collected in net; Sevier Co., Little River at the Sinks, 25 May 2001, rock holes; Chimney Tops trailhead (1066 meters, 35.6353°N, 83.4694°W), 16 July 2001, larvae, rock holes; Roaring Fork Motor Trail, 17 July 2001, rock holes.

Culex territans was the most commonly collected species of Culex in riverside rock holes. No biting records were established for Cx. territans ; however, it is believed to feed almost exclusively on amphibians and reptiles ( Barnard & Durden 2000). In host­preference tests it chooses reptiles and amphibians over mammals and birds ( Means 1968), and feeds on amphibians in preference to reptiles ( Irby & Apperson 1988). Two females captured in a net around the legs of a human at Cosby were probably not host seeking because they do not bite humans. Smith et al. (1994) implicated Cx. territans as a vector of Hepatozoon sipedon to water snakes ( Nerodia sipedon ) and leopard frogs ( Rana pipiens ). Culex territans also is the vector of H. catesbianae Stebbins to bull frogs ( Rana catesbeiana Shaw ) ( Smith 1996).

Culiseta inornata (Williston)

Collections: North Carolina, Haywood Co., Purchase Knob (1529 meters, 35.5918°N, 83.0602°W), 26 October–21 November 2001, Malaise trap, coll. Parker, Stocks, & Petersen; Swain Co., Andrews Bald, 20 October–13 November 2000, Malaise trap, coll. Parker, Stocks, & Petersen.

Culiseta inornata was trapped late in the year at elevations greater than 1000 meters, indicating that it probably overwinters as an adult and is active at near­freezing temperatures. It feeds on lagomorphs and deer and transmits Snowshoe Hare and Jamestown Canyon viruses ( Foster & Walker 2002). Culiseta inornata is a potential vector of West Nile virus and other arboviruses.

Ochlerotatus atropalpus (Coquillett)

Collections: North Carolina, Haywood Co., Big Creek , 17 May 2001, adults swarming at car radiator; Swain Co., Oconaluftee/Ravensford, 7 August 2002, landing and probing on feral cat; Tow String Road, 15 August 2001, larvae, rock pools; Tennessee, Little River at the Sinks, 25 May 2001, biting human, 17 June 2001, 23 November 2001; Chimney Tops trailhead, 9 September 1999, larvae, rock pool.

Ochlerotatus atropalpus is a native rock­pool mosquito. Females are autogenous for the first ovarian cycle but require blood meals for additional egg batches. Ochlerotatus atropalpus is usually not a pest except in areas adjacent to larval habitats. Biting records on humans and a feral cat indicate that this mosquito could be a potential vector of zoonotic pathogens. It can vertically transmit St. Louis encephalitis virus ( Pelz & Freier 1990). Ochlerotatus japonicus , a recently introduced rock­hole mosquito, might invade the Park and compete with Oc. atropalpus .

Ochlerotatus canadensis (Theobald)

Collections: North Carolina, Swain Co., Noland Creek (518 meters, 35.4534°N, 83.5282°W), 23 May 2001, biting human; Oconaluftee/Ravensford, 23 May 2001, biting human, 9 March 2002, leaf­lined pool; swamp at Payne Branch, 16 May 2002, biting human; Tow String Road, 9 March 2002, rock pools; Tennessee, Blount Co., Cades Cove, 23 April–8 May 2001, Lingren funnel, coll. Parker, Stocks, & Petersen.

Ochlerotatus canadensis is an aggressive biter of humans during the early spring, feeding in daylight along streams and in campsites. Ochlerotatus canadensis feeds on reptiles ( Barnard & Durden 2000). Wright & DeFoliart (1970a) collected blood­engorged Oc. canadensis from deer, beavers, raccoons, red foxes, opossums, cottontail rabbits, woodchucks, gray squirrels, fox squirrels, eastern chipmunks, ground squirrels, Peromyscus spp., chickens, woodcocks, snapping turtles, Blandings turtles, fox snakes, leopard frogs, and painted turtles in Wisconsin. Nasci et al. (2000) isolated LaCrosse encephalitis virus from pools of Oc. canadensis in West Virginia.

Ochlerotatus hendersoni Cockerell

Collections: North Carolina, Fontana Dam (525 meters, 35.4732°N, 83.4295°W), 8 July 2001, larvae, treehole near dam; Tennessee, Blount Co., Rich Mountain Trail, 9 September 1994, fogged from trees, coll. unknown; Sevier Co., Park Headquarters, 6 September 1999, hand collections, coll. D. DeFoe; Steep Branch near US 441 (914 meters, 35.6388°N, 83.5082°W), 16 July 2001, biting human.

Ochlerotatus hendersoni is a tree­hole mosquito that closely resembles Oc. triseriatus . Both species are potential vectors of viruses, including LaCrosse encephalitis virus, and filarial nematodes in the Park. Ochlerotatus hendersoni usually develops higher in trees than does Oc. triseriatus .

Ochlerotatus sticticus (Meigen)

Collections: North Carolina, Swain Co., Oconaluftee /Ravensford, 9 March 2002, woodland pool, larvae; Tennessee, Sevier Co., Little River at the Sinks, 24 March 2000, biting human.

Ochlerotatus sticticus is an early­spring mosquito that develops in spring ponds and shallow leaf­filled pools. This mosquito will bite humans. Wright & DeFoliart (1970a) collected blood­engorged Oc. sticticus from deer, beavers, raccoons, red foxes, opossums, cottontail rabbits, woodchucks, gray squirrels, fox squirrels, eastern chipmunks, ground squirrels, Peromyscus spp., chickens, woodcocks, snapping turtles, Blandings turtles, fox snakes, and painted turtles in Wisconsin.

Ochlerotatus triseriatus (Say)

Collections: North Carolina, Haywood Co., Big Creek ranger station, 17 August 2001, biting human; Cataloochee, 22 July 2002, biting human; Purchase Knob, 14 May 2002, larvae, treehole; Swain Co., Tow String Road, 8 July 2002, larvae in treehole; Twentymile Creek, 16 May 2002, larvae in treehole; Payne Branch, 16 May 2002, exuviae, treehole near creek, 8 July 2001, biting human; Mount Weaver overlook on US 441 (1466 meters, 35.5979°N, 83.4216°W), 15 August 2001, biting human; Oconaluftee/Ravensford, 9 June 2001, larvae in treehole; 9 June 2001, larvae treehole; Tennessee, Blount Co., sinking stream at mouth of Bull Cave (549 meters, 35.6442°N, 83.8077°W), 17 June 2001, biting human; Cades Cove, 11 June 2002, biting human; Cocke Co., Cosby Nature Trail, 29 May 2001, larvae in treehole; Sevier Co., Roaring Fork motor trail, 16 July 2001, biting humans; Goshen Prong, 5–12 November 2001, Malaise trap, coll. Parker, Stocks, & Petersen; Park Headquarters, unknown date, coll. D. DeFoe.

Ochlerotatus triseriatus is potentially the most significant human­biting mosquito in the Park. Although it is not always the dominant human biter, it is present throughout most of the year. It is also the primary vector of LaCrosse encephalitis virus ( Nasci et al. 2000), a potentially serious arbovirus. LaCrosse encephalitis is endemic in Cherokee, NC and Cosby, TN ( Anonymous 1990; Gottfried et al. 2002), and thus is in the Park. Barnard & Durden (2000) noted that this mosquito feeds on reptiles.

Psorophora columbiae (Dyar & Knab)

Collections: North Carolina, Swain Co., Job Corps area (617 meters, 35.5230°N, 83.3055°W), 15 August 2001, ditch along road; Oconaluftee/Ravensford, 28 August 2001, light trap, coll. R. Harrington & D. Jones.

Most species of Psorophora oviposit in pools that flood after strong rains or along streams that overflow. Because the majority of the Park is steep and relatively undisturbed, the area is not conducive to development of Psorophora species. Psorophora columbiae is implicated as a vector of Potosi virus in South Carolina by Wozniak et al. (2001). It fed on canids, pigs, deer, and rabbits in North Carolina ( Irby & Apperson 1988) .

Toxorhynchites rutilus (Coquillett)

Collections: North Carolina, Haywood Co., Purchase Knob , 23 July 2002, bog; Swain Co., Mount Buckley, 3 July 1991, hand collection, coll. R. Cagnon; Oconaluftee/Ravensford, 8 July 2002, treehole; Tennessee, Blount Co., Cades Cove, 27 August–10 September 2001, Malaise trap, coll. R. Hightower & J. Burbank; Cocke Co., Cosby, 17 August 2001, treehole, pupa; Sevier Co., near Gatlinburg, 31 August 1939, adult, coll. A. Stupka.

Toxorhynchites rutilus is not a blood­feeding mosquito but has been included for completeness. It is predatory on other mosquitoes and was found most often in treeholes with Oc. triseriatus .