Culicoides (Haematomyidium) stellifer (Coquillett)

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 : 68-70

Culicoides (Haematomyidium) stellifer (Coquillett) (new status)

(Fig. 134, 135, 189)

Ceratopogon stellifer Coquillett, 1901: 603 (key; female; District of Columbia).

Culicoides stellifer (Coquillett) : Kieffer 1906: 55 (combination). Malloch 1915: 300 (key; male, female; distribution; fig. male wing). Hoffman 1925: 295 (key; female; fig. wing, mesonotum). Root and Hoffman 1937: 162 (key; female; male genitalia; fig. male genitalia). Fox 1942: 419 (pupa; fig. respiratory trumpet, female anal segment). James 1943: 148 (seasonal distribution; Colorado). Knowlton and Fronk 1950: 114 (Utah: Cache County). Knowlton and Kardos 1951: 163 (Utah: Kane County). Wirth 1952a: 184 (key; male genitalia; fig. dorsal thoracic pattern, aedeagus). Bullock 1952: 20 (key; female; male genitalia; biology; seasonal distribution; Utah: Salt Lake County). Rees and Bullock 1954 (Utah: Salt Lake County). Foote and Pratt 1954: 32 (key; diagnoses of female, male, pupa; fig. female wing, mesonotum, palpus, male genitalia).

Culicoides (Oecacta) stellifer: Khalaf 1954: 37 (assignment to subgenus Oecacta ). Fox 1955: 255 (key and diagnoses of subgenera; species key; taxonomy). Wirth and Bottimer 1956: 263 (Texas ecology). Forattini 1957: 421 (key; female; male genitalia; fig. female eyes, flagellomeres 8–9, palpus, mesonotum, wing and wing variation, male genitalia, aedeagus, parameres, pupal anal segment, respiratory trumpet; distribution map). Jamnback 1965: 99 (key; female; male genitalia; pupa, larva; biology; fig. male genitalia, female wing, antenna, palpus, eye separation, pupa, larva). Atchley 1967: 992 (key; numerical characters; female; male genitalia; fig. female wing, palpus, tibial comb, spermathecae, male genitalia, parameres). Childers and Wingo 1968: 18 (key; biology; fig. female wing, spermathecae). Battle and Turner 1971: 81 (female; male genitalia; larval habitats; feeding habits; seasonal distribution; fig. female eye separation, palpus, wing, spermathecae, male genitalia, parameres). Blanton and Wirth 1979: 149 (key; numerical characters; female; male genitalia; pupa, larva; fig. female antenna, palpus, wing, eye separation, spermathecae, leg, male genitalia, parameres; larval habitat; feeding habits; seasonal distribution). Wirth et al. 1985: 28 (numerical characters; fig. female wing). Murphree and Mullen 1991: 352 (key; larva; numerical characters; fig. thorax, epipharynx, mandible, hypostoma, caudal segment).

Culicoides (Haematomyidium) stellifer: Vargas 1960: 42 (assignment to subgenus Haematomyidium ).

Diagnosis. ( Tables 14, 15) Brown; wing pattern distinct; r 2 dark; three pale spots past end of costa in r 3, the first at tip of costa bilobed 8-shaped and not extending to M 1 or r-m crossvein, the second a crude C-shape almost always connected along anterior wing margin to a small third spot at apex of cell to form an arch; three irregular pale spots in m 1, sometimes conjoined narrowly along posterior margin of cell; m 2, cua 1 with pale spots; M 1 and M 2 without pale spots; two pale spots in distal half of anal cell, the second reaching wing margin, on male the spots merged forming a lobed spot reaching wing margin; male tergite 9 apicolateral processes as long as ~0.4 the distance between them; ventral apodeme of gonocoxite with two well-developed widely divergent processes, footlike; aedeagus simple, median process tapering to blunt minutely serrate tip, aedeagal ratio ~0.6; parameres separate, with blunt submedian lobe smaller than width of paramere, and with subapical fringe of spines. (Male genitalia indistinguishable from that of C. kettlei Fig. 80 .)

Distribution. North America from Idaho, Montana to Nova Scotia, south to California, Florida, Mexico, Trinidad, Venezuela. Utah: Box Elder, Cache, Garfield, Grand, Kane, Salt Lake, Summit counties.

Larval ecology. Immatures have been collected or reared from ooze from tree wounds ( Wirth 1952a), heavily vegetated and bare moist mud with rotting leaves at pond margins, a shaded stream margin with decaying leaves ( Williams 1955), mud at pond margins ( Wirth and Bottimer 1956), shallow stream-edge depressions with decaying leaves ( Murray 1957), freshwater soil ( Jones 1961b), moist alkaline dung-polluted sunlit soil, leaves in stream and pond margins, buckeye ( Aesculus octandra ) treeholes ( Hair et al. 1966), sand bank of pool adjacent to creek ( Childers and Wingo 1968), and muddy lake, pond, marsh, and stream margins often with wet leaves and grass ( Blanton and Wirth 1979). In laboratory studies, Erram and Burkett-Cadena (2018) determined C. stellifer prefers to oviposit on low-organic mud and Sphagnum moss rather than field water- or manure-polluted mud.

Erram et al. (2019) reared C. stellifer from mud substrate samples collected over three months in Florida from the edges of puddle, seepage, and stream habitats, which produced 94, 12, and 10 adults, respectively. They also characterized the samples for P, K, Mg, Ca, Cu, Mn, Zn, organic matter, pH, moisture, electrical conductivity, and microbes and found that adult production in the puddle samples was correlated (in descending order of importance) positively with K and Zn concentrations and negatively with pH, P concentration, electrical conductivity, Mg concentration, and organic matter.

Life cycle. When experimenting with rearing C. stellifer in the laboratory at 26 °C, Erram and Burkett-Cadena (2020) found development took an average of 28 d from oviposition to adult emergence when reared on agar with nematodes as the food source; and survivorship was 38%. The egg stage lasted 3–4 d with a 56% hatch rate. The larval stage lasted an average of 21 d with 71% survival to pupation, which lasted an average of 3.5 d with 95% survival to adult emergence.

Adult behavior. Murray (1957) reported C. stellifer to be day-biters and most active in lowland fields and pastures in Virginia. However, Blanton and Wirth (1979) said this record likely refers to Culicoides paraensis (Goeldi) ; and Hair (1966) found flight activity in Virginia was through the night, greatest during 2100–2400 hours, then tapering off to 0600 hours. Furthermore, Murray’s habitat distinctions may be biased by his use of light traps, which are more effective in open areas. Possibly clarifying this, Swanson and Adler (2010), using CO 2 -baited unlit traps, collected 10% of their C. stellifer at 1.5 m, 77% at 5 m, and 12% at 10 m up in the forest canopy; and McGregor et al. (2018) found C. stellifer significantly more abundant in UVLTs 6–9 m up rather than at groundlevel within the forest—a distinction Murray did not make. In addition, Sloyer (2018), using light traps with and without CO 2, characterized 23 Florida habitat variables for temperature, precipitation, and vegetation for predicting C. stellifer host-seeking activity; however, the results are of limited usefulness in the generally more arid and higher altitude southwestern United States.

Culicoides stellifer is mostly mammalophilic. Known hosts are human ( Bullock 1952; Hair 1966; Reeves et al. 2004; Sloyer et al. 2019a), goat, turkey ( Humphreys and Turner 1973), cow ( Schmidtmann et al. 1981; Zimmerman and Turner 1983; Mullen et al. 1985a), sheep ( Zimmerman and Turner 1983), blue jay ( Cyanocitta cristata ) ( Garvin and Greiner 2003), white-tailed deer ( Odocoileus virginianus ) ( Mullen et al. 1985a; Smith and Stallknecht 1996; Hopken et al. 2017; McGregor et al. 2018; Sloyer et al. 2019a), raccoon ( Procyon lotor [Linnaeus], Procyonidae ), eastern gray squirrel ( Sciurus carolinensis ) ( McGregor et al. 2018), and chicken ( Gallus gallus ) ( Sloyer et al. 2019a). In Florida, McGregor et al. (2019c) found C. stellifer prefers to feed on red deer ( Cervus sp. ) and fallow deer ( Dama dama [Linnaeus], Cervidae ) rather than Bovidae and white-tailed deer.

Hair (1966) collected blood-engorged C. stellifer from drop traps baited with domestic rabbit, eastern cottontail rabbit ( Sylvilagus ), guinea pig ( Cavia porcellus ), opossum ( Didelphis ), and turkey ( Meleagris gallopavo ). Gerhardt (1986) collected C. stellifer from white-tailed deer and cow-baited drop traps. Schmidtmann et al. (1981) reported C. stellifer strongly preferred biting calves on the belly instead of on the head, back, or legs. Wieser-Schimpf et al. (1991) compared collections from New Jersey UVLTs with and without CO 2 in Louisiana and found those with CO 2 collected a greater but statistically insignificant number of nulliparous, parous empty, engorged, and gravid females.

Vector potential. Culicoides stellifer has been found naturally infected with vesicular stomatitis New Jersey virus (VSV) (Vesiculovirus, Rhabdoviridae ) ( Walton et al. 1987, Kramer et al. 1990), bluetongue virus (BTV) ( Mellor et al. 2000; McGregor et al. 2019b; Becker et al. 2020), West Nile virus (WNV) ( Sabio 2005; Sabio et al. 2006), and epizootic hemorrhagic disease virus (EHDV) ( McGregor et al. 2019b). The infection rates and estimated concentrations of WNV were similar to those known for mosquito vectors of WNV. Mullen et al. (1985b) demonstrated female C. stellifer could be infected by intrathoracic inoculation and harbor BTV, though the experiment did not prove C. stellifer ’s ability to be naturally infected with BTV. More recently, McGregor et al. (2019b) collected C. stellifer , with no visible blood in the gut, infected with EHDV and BTV retained from feeding on white-tailed deer, fallow deer, and elk ( Cervus spp. ) during EHDV and BTV episodes in Florida. Furthermore, if C. stellifer is found to be a competent vector, its May to September seasonal distribution in both Grand County (Table 5) and Salt Lake County ( Bullock 1952) would likely give it an important role in transmitting EHDV and BTV in the western United States.

Symbionts. Culicoides stellifer is sometimes heavily parasitized by mermithid nematodes, which produce intersexes in surviving adult midges. Smith and Perry (1967) collected 44 mermithid-induced intersexes (27% of males) in Florida, with intersex rates up to 62%; Wieser-Schimpf et al. (1991) collected 31 intersexes (2% of total males and females) in Louisiana, but did not check for parasitism; and, Erram et al. (2019) found 5% of the adults reared from puddle samples collected over three months in Florida were mermithid-parasitized intersexes. Another symbiont study ( Erram 2016) found that the bacterial flora on adult female C. stellifer consisted predominately of Proteobacteria—likely because of its relatively unpolluted larval habitat.

Remarks. North American authors ( Blanton and Wirth 1979; Wirth et al. 1985; et al.) and the most recent catalog ( Borkent and Dominiak 2020) list C. stellifer in subgenus Oecacta Poey , whereas European authors ( Meiswinkel et al. 2004; EFSA 2009) follow Vargas’s (1960) placement of C. stellifer in subgenus Haematomyidium . Because of the close similarity of C. stellifer to C. (Haematomyidium) kettlei (see C. kettlei remarks), because of the closer similarity of the male genitalia of C. stellifer to that of C. paraensis (the subgenus Haematomyidium type species) than to that of Culicoides furens (Poey) (the subgenus Oecacta type species), and because Forattini (1957) keys C. stellifer and C. paraensis to the same terminal couplet in his subgenus Oecacta key, I am following Vargas’s (1960) assignment of C. stellifer to subgenus Haematomyidium (new status) Furthermore, of the 152 species of subgenus Oecacta listed in Borkent and Dominiak (2020), only C. stellifer has a Nearctic type and only six ( Culicoides alahialinus Barbosa , Culicoides barbosai Wirth and Blanton , Culicoides cancer Hogue and Wirth , C. furens , Culicoides furensoides Williams , and Culicoides gorgasi Wirth and Blanton ) have Neotropical types, indicating subgenus Oecacta is presently a predominantly Afro-Eurasian assemblage.

Mitochondrial DNA CO1 gene sequences suggest C. stellifer is a species complex ( Shults et al. 2020). Specimens from Texas, South Carolina, and Florida showed relatively little genetic divergence between populations, whereas specimens from Ontario clustered in a divergent genetic group more in accordance with that of a different species.

Subgenus Monoculicoides Khalaf

Figures

Figures 79–80. Male genitalia of Culicoides, ventral view, basal arms of aedeagus (Aa), submedian lobe on paramere (Pml), ventral apodeme of gonocoxite (Gcva), distal spines of paramere (Pds). 79) C. mohave, apex of aedeagus circled (San Bernardino County, CA [FSCA]). 80) C. kettlei (Riverside County, CA [BM]).