Culicoides (Beltranmyia) crepuscularis Malloch

Phillips, Robert A., 2022, Culicoides Latreille and Leptoconops Skuse biting midges of the southwestern United States with emphasis on the Canyonlands of southeastern Utah (Diptera: Ceratopogonidae), Insecta Mundi 2022 (907), pp. 1-214 : 51-54

Culicoides (Beltranmyia) crepuscularis Malloch

( Fig. 52 , 89 , 142, 143, 170–172)

Culicoides crepuscularis Malloch, 1915: 303 (male, female; fig. male genitalia, female wing; thoracic dorsum; Illinois). Hoffman 1925: 298 (key; female; fig. wing, mesonotum). Root and Hoffman 1937: 159 (key; female; male genitalia; fig. male genitalia). Thomsen 1937: 69 (key; larva, pupa; fig. respiratory trumpet). Fox 1942: 415 (pupa; fig. respiratory trumpet, female anal segment). James 1943: 149 (seasonal distribution: Colorado). Knowlton and Fronk 1950: 114 (Utah: Cache, Garfield counties). Knowlton and Kardos 1951: 163 (Utah: Washington County). Wirth 1952a: 188 (key; female; male genitalia; fig. female wing, dorsal thoracic pattern, palpus). Bullock 1952: 13 (female; male genitalia; habitat and biotic associations; seasonal distribution; Utah: Salt Lake County). Rees and Bullock 1954 (Utah: Salt Lake County). Foote and Pratt 1954: 19 (key; diagnoses of female, male, pupa; fig. female wing, mesonotum, spermatheca, palpus, male genitalia).

Culicoides (Beltranmyia) crepuscularis: Vargas 1953: 33 (subgenus Beltranmyia Vargas ; designated C. crepuscularis as type species). Fox 1955: 233 (key and diagnoses of subgenera; species key; taxonomy). Williams 1956: 299 (key; Bermuda). Wirth and Bottimer 1956: 263 (Texas ecology). Wirth and Williams 1957: 13 (key; diagnosis). Vargas 1960: 47 (fig. female wing, male genitalia). Jamnback 1965: 52 (key; female; male genitalia; pupa, larva; biology; fig. male genitalia, female wing, antenna, palpus, eye separation, pupa, larva). Atchley 1967: 972 (key; numerical characters; female; male genitalia; variation; fig. female wing, palpus, tibial comb, spermatheca, male genitalia, parameres; biology). Childers and Wingo 1968: 11 (key; biology; fig. female wing, spermathecae). Jorgensen 1969: 13 (quantitative characters; key; female, male; seasonal distribution; fig. female wings, palpus, spermatheca, antenna, head, male genitalia, parameres, head, intersex head). Battle and Turner 1971: 34 (female; male genitalia; larval habitats; feeding habits; seasonal distribution; fig. female eye separation, palpus, wing, spermathecae, male genitalia, parameres). Blanton and Wirth 1979: 75 (key; numerical characters; female; male genitalia; pupa, larva; fig. female antenna, palpus, wing, eye separation, spermatheca, leg, male genitalia, parameres; larval habitat; feeding habits; seasonal distribution). Downes and Wirth 1981: 415 (fig. male genitalia). Wirth et al. 1985: 30 (numerical characters; fig. female wing). Wirth et al. 1988: 56 (numerical characters; fig. female wing). Murphree and Mullen 1991: 356 (key; larva; numerical characters; fig. mandible, hypostoma, head, epipharynx, thorax). Brickle and Hagan 1999: (key; numerical characters; biology; Belize). Borkent and Spinelli 2000: 29 (in Neotropical catalog).

Culicoides (Monoculicoides) crepuscularis: Khalaf 1954: 40 (assignment to subgenus Monoculicoides Khalaf ).

Diagnosis. ( Tables 14, 15) Wing pattern distinct; r 2 dark; M 1 and M 2 dark except at fork; r 3, m 1, m 2 each with medial and distal ovoid pale spots, though the medial pale spot in m 1 or m 2 may be absent (see remarks); one sclerotized fully developed ovoid spermatheca with neck shorter than wide; ventral apodeme of gonocoxite lacking or merely an inconspicuous obtuse bump; aedeagus V-shaped, median process tapered blunt; parameres separate, apices simple pointed. (See remarks.)

Distribution. North America from southern Alaska and Canada (British Columbia to Nova Scotia), through the United States, Bermuda, Mexico, Belize, El Salvador, Honduras, Nicaragua, to Costa Rica. Utah: Grand, Salt Lake, Uintah, Washington counties.

Larval ecology. Bullock (1952) collected and reared immatures from spikerush ( Eleocharis acicularis [Linnaeus] Roemer and Schultes, Cyperaceae ) mats in Salt Lake County. Jones (1961b) collected pupae from an organic boggy area in direct sunlight in Garfield County, Utah, and from the nonvegetated sunlit margin of an alkaline stream near Cisco (47 km north-northeast of Moab), Grand County, along with immatures of a Stonei group species (as Culicoides stonei James ), C. occidentalis or C. sonorensis (as C. variipennis australis ), C. haematopotus (may be C. defoliarti ), C. grandensis (as “n. sp.”), and C. jamesi . I was able to rear C. crepuscularis along with C. sonorensis , C. occidentalis , and C. mortivallis from mud collected on 10 September 2020 from nonvegetated sunlit alkaline pools in a stream bed in Grand County at 38.96339°N 109.33585°W and 1315 m elevation in the same wash as Jones’s Cisco pupae collection site.

Culicoides crepuscularis immatures have been collected or reared from alkaline dung-polluted direct sunlit soil ( Hair et al. 1966), drainage ditches, freshwater seepage ponds ( Rowley 1967), mud flats ( Rowley 1967; Childers and Wingo 1968), high-organic fresh- to salt-marsh ( Blanton and Wirth 1979), muddy areas in pastures, mud contaminated by effluent from a milking parlor ( Kline and Greiner 1985), and in greatest abundance at the water’s edge of pond marshes, slow streams in meadows, and forest and grassland bogs with pH 6.2–9.5 and low to high salinity ( McMullen 1978).

Culicoides crepuscularis immatures often share habitats with other species. In particular, Jones (1967) collected pupae of C. crepuscularis , along with C. sonorensis (as C. variipennis ) and a species close to Culicoides wisconsinensis Jones , from 20 April into May, which had overwintered as larvae in mud in Weld County, Colorado; and Pfannenstiel and Ruder (2015) found C. crepuscularis along with C. sonorensis and C. haematopotus in mud in relict (long unused) and active bison ( Bison bison [Linnaeus], Bovidae ) wallows in Kansas about two weeks after they were flooded by rain.

Adult behavior. Culicoides crepuscularis is an opportunistic feeder on birds and mammals. Reported hosts are crow ( Corvus brachyrhynchos Brehm , Corvidae ), white-throated sparrow ( Zonotrichia albicollis [Gmelin], Passerellidae ), ruffed grouse ( Bonasa umbellus [Linnaeus], Phasianidae ), saw-whet owl ( Aegolius acadicus [Gmelin], Strigidae ) ( Bennett 1961; Fallis and Bennett 1961a), domestic duck ( Anas boschas Linnaeus ), American robin ( Turdus migratorius Linnaeus , Turdidae ), purple finch ( Haemorhous purpureus [Gmelin], Fringillidae ), blue jay ( Cyanocitta cristata [Linnaeus], Corvidae ), Canada jay ( Perisoreus canadensis [Linnaeus], Corvidae ) ( Bennett 1961), flicker ( Fallis and Bennett 1961a), starling ( Robinson 1961), magpie ( Pica pica hudsonia [Sabine], Corvidae ) ( Hibler 1963), grackle ( Quiscalus quiscula versicolor [Vieillot], Icteridae ) ( Robinson 1971), mourning dove ( Zenaida macroura [Linnaeus]) ( Greiner 1975), turkey ( Meleagris gallopavo Linnaeus ) ( Atkinson 1988), house finch ( Haemorhous mexicanus [Müller], Fringillidae ) ( Hopken et al. 2017), chicken ( Gallus gallus [Linnaeus]) ( Sloyer et al. 2019a), human ( Edmunds and Keener 1954; Snow 1955; Hair 1966; Hair and Turner 1968), cow ( Roberts 1965; Zimmerman and Turner 1983), raccoon, domestic rabbit ( Wright and DeFoliart 1970), sheep ( Zimmerman and Turner 1983), and eastern gray squirrel ( Sciurus carolinensis Gmelin , Sciuridae ) ( McGregor et al. 2018). Furthermore, Hair (1966) collected blood-engorged C. crepuscularis from drop traps baited with domestic rabbit ( Oryctolagus cuniculus ), guinea pig ( Cavia porcellus [Linnaeus]), rat ( Rattus ), chicken, turkey, mallard duck ( Anas boschas ), bobwhite quail ( Colinus virginianus [Linnaeus]), and mourning dove; and Hood and Welch (1980) collected C. crepuscularis from red-winged blackbird ( Agelaius phoeniceus [Linnaeus], Icteridae ) nests.

Edmunds and Keener (1954) reported crepuscular-biting with a peak 15–45 minutes after sunset, and Nelson and Bellamy (1971) reported flight activity in Kern County, California, July–September, peaked near dusk and gradually diminished through the night without a peak near dawn. However, in Weld County, Colorado, C. crepuscularis activity was similar but showed a secondary peak either just before dawn in the hotter months of June and July or after dawn in the cooler months of May and August–October ( Barnard and Jones 1980b).

Snow (1955) reported crepuscular-biting on humans in the forest canopy (rather than in the understory), which is behavior consistent with ornithophilic or arboreal mammalophilic preferences. However, Murray (1957) reported C. crepuscularis adults were most active in lowland fields and pastures rather than forested areas; but this habitat distinction may be biased by his use of light traps, which are more effective in open areas. Clarifying this, McGregor et al. (2018) found C. crepuscularis more abundant (40 of 40 specimens with UVLT) 6–9 m up in the forest canopy rather than at ground-level within the forest—a distinction Murray did not make.

Vector potential. Culicoides crepuscularis has been found naturally infected with: an unidentified filarial nematode of starlings ( Robinson 1961); Chandlerella quiscali Linstow (Nematoda: Filarioidea), a parasite of grackles ( Quiscalus quiscula ) ( Robinson 1971; Huizinga and Granath 1984); Splendidofilaria picacardina Hibler (Nematoda: Filarioidea) and Eufilaria longicaudata Hibler (Nematoda: Filarioidea), parasites of magpies ( Wirth and Hubert 1989); bluetongue virus (BTV) in Colorado ( White et al. 2005) and Louisiana ( Becker et al. 2010; Becker et al. 2020); and epizootic hemorrhagic disease virus (EHDV) in Texas ( Schoenthal 2015). Texas specimens have also been found infected with DNA identical to that of Chandlerella quiscali from an Illinois grackle and with DNA identical to that of the avian malarial parasite Haemoproteus sacharovi Novy and MacNeal (Aconoidasida: Haemoproteidae ) from an Arizona mourning dove ( Martin et al. 2019). They noted H. sacharovi is also vectored by the pigeon louse fly, Pseudolynchia canariensis (Macquart) ( Diptera : Hippoboscidae )—unusual in that the two vectors are in different Diptera suborders.

Bennett and Fallis (1960) found C. crepuscularis in Canada to be a natural vector of Haemoproteus Kruse (reported as Haemoproteus danilewskii Kruse by Santiago-Alarcon et al. 2012b) and experimentally found sporozoites in C. crepuscularis salivary glands 8 d after feeding on infected crows and white-throated sparrows ( Fallis and Bennett 1961a). In addition, they demonstrated experimental vectorial competence of C. crepuscularis for transmission of Haemoproteus fringillae Labbé ( Fallis and Bennett 1961b) ; and Greiner (1975) collected C. crepuscularis feeding on mourning doves when Haemoproteus was being transmitted among doves in Nebraska.

Experiments also support C. crepuscularis being a competent vector of filarial nematodes. Hibler (1963) demonstrated complete development of Eufilaria longicaudata and Splendidofilaria picacardina in C. crepuscularis after feeding on an infected magpie, and Robinson (1971) found active Chandlerella quiscali microfilaria in the head and mouthparts of 11 of 23 C. crepuscularis 10 d after feeding on an infected grackle.

Symbionts. Culicoides crepuscularis is sometimes heavily parasitized by mermithid nematodes, which often produce intersexes in surviving adult. Smith and Perry (1967) found eight of eight males collected with NJLTs in Florida were mermithid-induced intersexes ; Jorgensen (1969) collected 44 mermithid-induced intersexes (23% of males) in Washington, with intersex rates up to 74%; Wieser-Schimpf et al. (1991) collected 110 intersexes (50% of males) in Louisiana, but did not check for parasitism; and, Atchley (1967) collected two intersex specimens in New Mexico, however, he did not say if they were parasitized.

Eight of eleven male C. crepuscularis collected in Grand County 16 May 2002 were parasitized by larval mites ( Table 10). Three other mites were loose and may have come off any of the males or four females in that collection.

Erram (2016) studied the bacterial flora on adult female C. crepuscularis and found that Proteobacteria were predominant. In addition, Wolbachia infections, which can alter dipteran reproduction by killing male embryos, inducing gamete incompatibility, or feminizing genetic males ( Stouthamer 1999), have been found in a C. crepuscularis population in Florida ( Covey 2020), suggesting the possibility of using Wolbachia to control C. crepuscularis populations or reduce pathogen transmission.

Atypical biology. A specimen with diminished distal pale wing spots (Fig. 172) and having one normally large and two small ovoid spermathecae, 0.28 and 0.33 as long as the large spermatheca, was collected with UVLT on 16 July 2019 at 43.73340°N 114.27168°W and 1974 m elevation in Blaine County, Idaho.

Remarks. Across its extremely wide geographic range, considerable C. crepuscularis wing pattern variation has been documented by Atchley (1967) and figured in Wirth et al. (1985). Several specimens collected in the present study have reduced or lack distal pale spots in r 3, m 1, or m 2: two Blaine County, Idaho, females have greatly diminished wing spots (Fig. 172); the Bonneville County, Idaho, female in Figure 171 lacks the medial pale spot in m 2; and the Grand County male in Figure 143 lacks the medial pale spot in m 1. Also, the ventral apodeme of the gonocoxite illustrated from Florida specimens in Figure 55h of Blanton and Wirth (1979) is somewhat different from those illustrated from New Mexico specimens in Figure 33 of Atchley (1967) and collected in the present study ( Fig. 89 ). Culicoides crepuscularis may be a species complex, but further study would be needed.

Subgenus Diphaomyia Vargas

Figures

Figures 50–55. 50) Culicoides sonorensis male wing. 51) C. occidentalis male wing. Spermathecae. 52) C. crepuscularis. 53) C. grandensis (paratype). 54) C. sonorensis. 55) C. sonorensis, lateral view (anterior to left) of female mesonotum showing prescutal pit (presct pit) and dark patches around seta bases.

Figures 88–93. Male genitalia of Culicoides, ventral view. 88) C. luglani, submedian processes of parameres circled. 89) C. crepuscularis, ventral apodeme of gonocoxite circled. 90) C. calexicanus, apices of parameres circled, apex of aedeagus delineated. 91) C. hawsi (paratype, Modoc County, CA [FSCA]). 92) C. palmerae, sharp lateral shoulders on median process of aedeagus indicated (A). 93) C. utahensis.

Figures 33–36. 33) Culicoides moabensis female (top) and unidentified brown C. subgenus Selfia female (bottom), lateral habitus (in alcohol). Male genitalia, ventral view focused on aedeagus. 34) C. brookmani, basal arm of paramere (Pa), distal tip of median process of paramere delineated (Pt), basal arm of aedeagus (Aa), tip of median process of aedeagus (At), gonocoxite (Gc), gonostylus (Gs). 35) C. moabensis, median process of paramere (Pmp) (paratype). 36) C. denningi, sternite 9 caudal lobes (S9cl).