Culicoides (Sensiculicoides) kibunensis Tokunaga

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 : 84-86

Culicoides (Sensiculicoides) kibunensis Tokunaga

( Fig. 98 , 152, 231, 273)

Culicoides kibunensis Tokunaga, 1937: 298 (male, female; fig. female wing, antenna, male genitalia; Japan).

Culicoides (Oecacta) kibunensis: Khalaf 1954: 36 (assignment to subgenus Oecacta ). Arnaud 1956: 107 (female, male; fig. female head, antenna, palpus, mouthparts, mesonotum, wing, legs, tibial spines, spermathecae, genitalia, male antenna, palpus, mesonotum, wing, ventral genitalia, dorsal genitalia, parameres and aedeagus; synonyms: Culicoides ponkikiri Kono and Takahasi , Culicoides sitinohensis Okada ). Jorgensen 1969 (as species 75): 36 (key; quantitative characters; female; male genitalia; fig. female antenna, spermathecae, palpus, wing, male genitalia, parameres; seasonal distribution; Washington). Wirth and Blanton 1969a: 560 (female, male; fig. antenna, palpus, wing, eye separation, spermathecae, male genitalia, parameres; synonym: Culicoides cubitalis Edwards ). Wirth et al. 1985: 38 (numerical characters; fig. female wing).

Culicoides (Sensiculicoides) kibunensis: Szadziewski et al. 2016: 420 (resurrection and diagnosis of subgenus Sensiculicoides Shevchenko, 1977 ; placement of C. kibunensis in Sensiculicoides ).

Culicoides cubitalis Edwards, 1939 : Edwards et al. 1939: 40, 139 (male; fig. genitalia; Britain). Kettle and Lawson 1952: 438, 460 (larva, pupa; fig.). Campbell and Pelham-Clinton 1960: 244 (male, female). Callot and Kremer 1963: 113 (male, female, intersexes; numerical characters; fig. palpi, wings).

Culicoides ponkikiri Kono and Takahasi, 1940: 74 (key; female; fig. wing, antenna, palpus; Japan).

Culicoides sitinohensis Okada, 1941: 18 (female).

Culicoides albicans (Winnertz) , misidentified: Callot 1959: 439 (intersex; fig. female, head, male head; France).

Diagnosis. ( Tables 14, 15) Wing pattern reduced; r 2 dark; pale spots at tip of costa, on r-m crossvein, absent or faint in apices of r 3, m 1, m 2, cua 1; antennal ratio 1.13–1.65; proboscis ratio 0.74–0.90; palpal ratio 1.57–2.78;

spermathecae usually slightly unequal by 1.05× but up to 1.26× in some specimens, sclerotized necks shorter than wide or absent; sclerotized ring on spermathecal duct; ventral apodeme of gonocoxite simple; gonostylus almost straight, midportion of lateral contour concave; aedeagus Y-shaped, median process stout at base, tapering to blunt tip, sometimes with a pair of lateral finlike distally pointed processes at ~0.7 (these difficult to see), aedeagal ratio ~0.5; parameres separate, apices simple, pointed, curved ventrally.

Distribution. Holarctic; in North America: British Columbia ( Costello 1982), Washington, Oregon, Idaho (Blaine, Bonneville, Custer counties, new state record), California (new state record [ Monarch 2021]), Utah (Garfield, Grand, San Juan, Sanpete, Summit counties), Colorado, Arizona.

Larval ecology. McMullen (1978) found Travisi group (likely C. kibunensis ) immatures, along with C. palmerae James , in slightly acid to neutral semi-aquatic to aquatic habitats with “high organic content of plant origin” in British Columbia.

Vector potential. All of the reported host, parasite, and vector competency studies on C. kibunensis have been Eurasian, and much evidence has been accumulated to show C. kibunensis ’ ability to transmit avian protozoans. Bernotienė et al. (2019) found sporozoites of Haemoproteus pallidus Valkiūnas and Iezhova (hPFC1) (Aconoidasida: Haemoproteidae ), which is a parasite common in birds of the family Muscicapidae , in wild-caught C. kibunensis —confirming vector competency for the parasite. Furthermore, Žiegytė et al. (2021) found Haemoproteus minutus Valkiūnas and Iezhova (hTURDUS2, hTUPHI01) (Aconoidasida: Haemoproteidae ) sporozoites in the salivary glands of and DNA in the thoraxes of C. kibunensis collected using UVLTs and bird-baited traps during 19–28 June in Lithuania —confirming its vector competency for this parasite known to cause morbidity and mortality in a broad range of birds from South American and Australasian parrots ( Ortiz-Catedral 2019) to migratory and non-migratory European passerine birds ( Passeriformes), including Eurasian reed warblers ( Acrocephalus scirpaceus [Hermann]), icterine warblers ( Hippolais icterina [Vieillot]), Eurasian blue tits ( Parus caeruleus Linnaeus ), bearded reedlings ( Panurus biarmicus [Linnaeus]), dunnocks ( Prunella modularis [Linnaeus]), common blackbirds ( Turdus merula Linnaeus , Turdidae ), ring ouzels ( Turdus torquatus Linnaeus ) ( Synek et al. 2013), song thrushes ( Turdus philomelos Brehm ), and European robins ( Erithacus rubecula [Linnaeus], Muscicapidae ) ( Palinauskas et al. 2013).

Culicoides kibunensis has also been found infected with other protozoan parasites known to have alternate vertebrate hosts but for which vector competency has not been proven. Martínez-de la Puente et al. (2011) collected C. kibunensis from Spain infected with three lineages of Haemoproteus and the avian malaria Plasmodium Marchiafava and Celli (Aconoidasida: Plasmodiidae ) lineage CulPlas1; however, Plasmodium agamae Wenyon , a parasite of reptiles, is the only Plasmodium known to be transmitted by Culicoides ( Telford 1988) . Santiago-Alarcon et al. (2012a) collected C. kibunensis from Germany that had fed on blackcaps ( Sylvia atricapilla [Linnaeus], Sylviidae ) and were infected with the Haemoproteus lineage SYAT07—a strain known to infect blackcaps. Synek et al. (2013) collected, with bird-baited traps in the Czech Republic, C. kibunensis infected with three lineages of Haemoproteus , including lineage TURDUS 2. Santiago-Alarcon et al. (2013) found C. kibunensis naturally infected with Haemoproteus parabelopolskyi Kruse (a parasite of blackcaps), and H. minutus ( Palinauskas et al. 2013) . In addition, Bernotienė et al. (2019) detected Haemoproteus tartakovskyi Valkiūnas DNA, and Žiegytė et al. (2021) detected H. tartakovskyi (hSISKIN1) and Plasmodium vaughani Novy and Mac- Neal (pSYAT05) DNA in C. kibunensis collected in Lithuania. Though these findings were from European C. kibunensis and do not confirm any ability to transmit these parasites, because the type host for P. vaughani is the American robin ( Turdus migratorius Linnaeus , Turdidae ) ( Iezhova et al. 2005) and P. vaughani is known to infect other species of Nearctic passerine birds ( Herman 1944), they suggest that C. kibunensis may play an important role in vectoring avian protozoan parasites in North America.

Symbionts. Culicoides kibunensis has also been found infected by parasites not known to have alternate vertebrate hosts. Podlipaev et al. (2004) collected from a buzzard ( Buteo buteo Linnaeus , Accipitridae ) nest a female C. kibunensis infected with Herpetomonas ztiplika Podlipaev et al. (Kinetoplastida: Trypanosomatidae ). Callot (1959, as C. albicans ) and Callot and Kremer (1963, as C. cubitalis ) described intersexes of C. kibunensis naturally parasitized by mermithid nematodes. Rieb et al. (1982) collected from a fluvial mud bank in France, turquoisblue C. kibunensis larvae (as C. cubitalis ) infected with an iridovirus ( Iridoviridae ) fatal in the last (fourth) larval instar. Pagès et al. (2017) collected C. kibunensis in Spain infected with Wolbachia endosymbionts, which can alter dipteran reproduction by killing male embryos, inducing gamete incompatibility, or feminizing genetic males ( Stouthamer 1999); and Möhlmann (2019) collected C. kibunensis in the Netherlands infected with Wolbachia and “ Candidatus Cardinium ”, another endosymbiont that may alter reproduction in Culicoides (Pilgrim et al. 2020) .

Adult behavior. Palearctic hosts of C. kibunensis include pig, goat, fowl ( Nishijima 1964), cow ( Bos taurus ), marsh warbler ( Acrocephalus palustris [Bechstein], Acrocephalidae ), common wood pigeon ( Columba palumbus Linnaeus , Columbidae ), yellowhammer ( Emberiza citrinella Linnaeus , Emberizidae ) ( Lassen et al. 2012), blackcap ( Sylvia atricapilla ), human ( Santiago-Alarcon et al. 2012a), and European robin ( Erithacus rubecula ) ( Santiago-Alarcon et al. 2013). In addition, engorged C. kibunensis were collected from great tit ( Parus major Linnaeus , Paridae ) and European pied flycatcher ( Ficedula hypoleuca [Pallas], Muscicapidae ) nest boxes ( Žiegytė et al. 2021). The broad range of Palearctic hosts and vector competency for transmission of avian parasites suggest C. kibunensis likely plays a similarly important role in North America.

Remarks. James’s (1943: 150) description of the aedeagus of a Colorado Culicoides simulans Root and Hoffman seems to be that of C. kibunensis instead of C. travisi , but because I have not seen the specimen, I am not proposing a new synonymy.

Wirth and Blanton (1969a: 562) state C. kibunensis is closely related to C. travisi , which can be distinguished from C. kibunensis “by the usual presence of marginal wing spots and in the male by the much shorter basal arch and long slender median process with parallel sides in the aedeagus”. However, the female wing photographs in Wirth et al. (1985: 39) show marginal wing spots in C. kibunensis intermediate between the reduced pattern of C. travisi on the same page and the more pronounced pattern of C. travisi in Blanton and Wirth (1979: 187); Battle and Turner (1971: 84) state for C. travisi , “pale spots rarely present along margin”; Jamnback (1965: 106) states for C. travisi the distal spots “often not apparent”; and a Virginia specimen lacks the marginal wing spots (Fig. 232). Hence, the wing pattern distinction is not reliable.

Furthermore, critical quantitative characters for the two species overlap ( C. kibunensis first, C. travisi second): antennal ratio (1.13–1.65, 1.39–1.68), palpal ratio (1.57–2.78, 2.09–2.70), proboscis ratio (0.74–0.90, 0.74–0.85) (data compiled from Jamnback 1965, Jorgensen 1969, Battle and Turner 1971); and leg-banding are nearly identical ( Table 15).

This leaves the size differential of the spermathecae as the only consistently described distinction for females. However, an Idaho specimen has an antennal ratio of 1.22 but a 1.26× spermathecal size differential, and similar discrepancies exist with other specimens.

For males, the only remaining described distinction is the shape of the aedeagus. Figure 65G for C. kibunensis in Arnaud (1956) shows a pair of lateral finlike distally pointed processes at ~0.7 on the median process of the aedeagus not shown or mentioned in any other references for either C. kibunensis or C. travisi . Only one of the slide-mounted specimens in the present study unambiguously had this characteristic. The others have aedeagi that otherwise are intermediate between those illustrated for the two species or more closely resemble those of C. kibunensis . Altogether, these overlapping characteristics may represent either hybridization between C. kibunensis and C. travisi or intraspecific variation of a single species and suggest the need for clarification of their species status (see also C. travisi remarks).

Figures

Figures 94–99. Male genitalia of Culicoides, ventral view. Ventral apodeme of gonocoxite and apex of paramere circled on Fig. 94–96. 94) C. sublettei (Gillespie County, TX [FSCA]). 95) C. usingeri. 96) C. vetustus (San Bernardino County, CA [BM]). 97) C. posoensis (paratype, Kern County, CA [FSCA]). 98) C. kibunensis. 99) C. travisi (VA [FSCA]).

Figures 63–65. Male genitalia of Culicoides subgenus Avaritia, ventral view. Upper images focused on aedeagus (A). Lower insets focused on caudal margin of tergite 9. Ventral apodeme of gonocoxite labeled (Gcva). Anteriordirected median process of aedeagus circled. 63) C. boydi (Riverside County, CA [BM]). 64) C. chiopterus (MD [FSCA]). 65) C. obsoletus (MD [FSCA]).