Culicoides Latreille

Borkent, Art, 2014, The Pupae of the Biting Midges of the World (Diptera: Ceratopogonidae), With a Generic Key and Analysis of the Phylogenetic Relationships Between Genera, Zootaxa 3879 (1), pp. 1-327 : 49-51

Culicoides Latreille

( Figs. 2F , 3A–C , 4A–C , 5A–B , 13B , 15A , 19A–D , 24A , 29K–L , 32G , 34F , 43H–N , 48A , 57A , 73H )

DIAGNOSIS: Only pupa of Ceratopogonidae with a prothoracic extension extending from the palpus to the antenna ( Fig. 24A ), the halter and hind leg slightly separated or barely touching ( Figs. 3B , 32G ), and the dorsal apotome relatively flat ( Figs. 19A–D ) and without a central dome-like protuberance (bearing the sensilla) (as in Figs. 19H–J ) and with or without spicules but if with a lateral row of stout, pointed spicules then also with further stout spicules more medially.

DESCRIPTION: Habitus as in Figs. 3A–C . Total length = 1.56–3.13 mm. Without larval exuviae retained on abdomen. Exuviae with flagellum appressed against lateral margin of face ( Fig. 15A ). Ecdysial tear medial to base of antenna ( Figs. 15A , 79D ); along prothoracic extension. Head: Dorsal apotome ( Figs. 19A–D ), without ventral line of weakness, with or without dorsomedial tubercle, without central dome; dorsolateral cephalic sclerite ( Fig. 13B ) separated from scutum by thin cuticle, separate from scutum upon emergence, each side separated medially by dorsal apotome in whole pupa; mouthparts ( Fig. 24A ) with mandible, lacinia well-developed, overlapping; palpus extending equal to or posterior to posterolateral margin of labium; labium separated medially by labrum, hypopharynx; apex of antenna ( Fig. 34F ) anterior to posterior extent of midlength portion of midleg (portion lateral to mesosternum); sensilla: dorsal apotomals ( Figs. 19A–D )—1 moderate to elongate seta, 1 campaniform sensillum; dorsolateral cephalic sclerite sensilla—2 setae, 1 campaniform sensillum; clypeal-labrals ( Fig. 24A )—0–2 setae; oculars ( Fig. 24A )—2 elongate setae, 1 campaniform sensillum. Thorax: Prothoracic extension ( Fig. 24A ) wide, well-developed, extending from palpus to antenna; mesonotum with short tubercles, not extending posteromedially but with metathorax having medially split to extending posteromedially, completely dividing metathorax medially ( Fig. 48A ); respiratory organ ( Figs. 43H–N ) length/width = 3.82–8.13, elongate, slender, circular in cross-section, with pores closely abutting or slightly separated at apex of respiratory organ, arranged in single straight or curved row or two widely spaced rows, with or without additional, more basal pores, outer surface with or without annulations, with or without spicules, with elongate, slender pedicel, base with short, strung out posteromedial apodeme, membranous base of respiratory organ short to moderately elongate, tracheal tube straight to slightly curved along length, with spirals restricted to base, distally with reticulations or plates; wing ( Fig. 34F ) with apical tubercle or angle lateral to apex of hind leg, separated medially by fore-, midlegs; halter apex and hind leg ( Fig. 32G ) just separate to just touching; halter apex abutting anterolateral knob-like extension of tergite 2; legs ( Fig. 34F ) with lateral margin of foreleg near midlength of wing evenly curved; hind leg visible at lateral margin of wing ( Fig. 32G ); with apex of foreleg moderately anterior to apex of midleg; apex of hind leg slightly dorsal to, partially abutting apex of midleg laterally; sensilla: anteromedials—1 seta; anterolaterals—2 setae, 1 campaniform sensillum; dorsal setae ( Figs. 29K–L )—D-1-T, D-2-T, D-4-T, D-5-T setae, D-3-T campaniform sensillum, D-3-T posterior to D-4-T; supraalar 2—campaniform sensillum; metathoracics ( Fig. 48A )—1 seta, 2 campaniform sensilla; M-3-T near anterior margin of metathorax. Abdomen: without pigmentation pattern or with tergites 1–7 with pair medially and pair anterolaterally (fading posteriorly) or tergites 2–7 with medial group of 3 and anterolateral pair, sternites 3–7 with medial stripe, anterolateral spot, or 2 pairs, fading posteriorly, segment 2 as wide or slightly wider than segment 3, segments with undivided, thin to thick setae, with rounded to pointed, short tubercles, tergites or sternites entire, each without membranous disc; segment 9 ( Fig. 73H ) not strongly modified, terminal processes closely approximated basally, each projecting posteriorly to posterodorsolaterally, tapering to pointed apex; sensilla: tergite 1 ( Fig. 48A ) with 7 setae, 2 campaniform sensilla, including 3 lateral sensilla, D-2-I, D-3-I closely approximated, D-7-I situated anteriorly near D-2-I, D-3-I; segment 4 ( Fig. 57A )—D-2-IV, D-3-IV short to moderately elongate setae on short tubercles; D-5-IV (rarely absent), D-8- IV, D-9-IV short to moderately elongate setae (D-9-IV absent in some), D-5-IV, D-4-IV, D-7-IV, D-8-IV, D-9-IV on short to moderately elongate, separate tubercles, in transverse row, arranged medially to laterally: D-5-IV, D-4-IV, D-7-IV, D-8-IV, D-9-IV; L-1-IV short seta on short to pointed tubercle, well anterior of posterior lateral setae, L-2- IV, L-3-IV, L-4-IV setae of variable length, on short to pointed tubercles, V-5-IV, V-6-IV, V-7-IV short to moderately elongate setae on rounded tubercles; segment 8 without D-3-VIII, without L-1-VIII; segment 9 ( Fig. 73H )—with D-5-IX, D-6-IX campaniform sensilla.

DISTRIBUTION AND HABITAT: The genus Culicoides is known from 1343 species from every Region worldwide ( Borkent 2014 ) but is notably absent from New Zealand. Immatures are present in a wide array of habitats but generally are associated with small and limited aquatic or very wet microhabitats. They are diverse and common in mud or decaying substrate on the margins of pools, swamps, ponds, streams and rivers, but are also found in such diverse habitats as damp or wet decomposing vegetation, wet leaf packs, manure, fungi, sap from wounds on trees, phytotelmata, seed husks, dead cacti, crab holes, springs, seeps, bogs, saline pools, fens, mangrove swamps, salt marshes, and river bottom (one species).

TAXONOMIC DISCUSSION: There are 226 species of Culicoides known as pupae ( Tables 2–3 ). Some of these, however, are poorly described, or are questionably associated (in part, because some adults are difficult to identify accurately). Furthermore, some authors have described differences between species which are now considered synonyms, likely indicating problems either with identification of the adults or the real possibility that more than one species is present under that name ( Thienemann 1928, Mayer 1934a, Lenz 1934, Dzhafarov 1964).

Many using this work will primarily want to identify pupae of Culicoides to genus. Aside from the features in the key and the diagnosis above, members of this genus have a nearly unique arrangement of the dorsolateral cephalic sclerite setae, with one long and the other quite small (in most species and difficult to see) to equally long. Pupae of Paradasyhelea also have this arrangement but they are relatively rare taxa restricted to Southern Hemisphere localities as well as the Olympic Peninsula in Washington, USA. In areas of sympatry, the arrangement of the spicules on the dorsal apotome will serve to distinguish the two genera. Nearly all other Ceratopogoninae have only one dorsolateral cephalic sclerite seta. Of the exceptions, Baeodasymyia , rare and restricted to the Neotropical Region, has two setae but also has a respiratory organ with a distinctive separate, short, expanded apical portion bearing pores in a single plane ( Fig. 44C ), some Parabezzia (e.g. P. petiolata ) have both setae very short and peg-like, and one specimen of Serromyia has both setae very short and slender.

Members of Culicoides may also be recognized by a combination of the halter and hind leg slightly separated or barely touching ( Figs. 3B , 32G ) and D-7-I placed anteriorly on tergite 1, near D-2-I and D-3-I.

There are various keys to species of pupae of Culicoides which include species from a given area or of a select species group, as follows (arranged geographically, New World to Old World, north to south):

- Jones (1955) — Wisconsin, USA.

- Jamnback (1965) — New York, USA; described the differences between subgenera and some species groups.

- Blanton & Wirth (1979) —Florida, USA; described the differences between subgenera and some species groups.

- Jones (1961) —to 13 Nearctic species.

- Atchley (1970) —Nearctic species of C. ( Selfia ).

- Jamnback & Wirth (1963) —eastern Nearctic species of obsoletus species group.

- Kann (1980) —Nearctic species of guttipennis species group, noting differences of the species group with other groups of Culicoides .

- Lamberson et al. (1992) —tree-hole species from eastern North America.

- Thienemann (1928) —northern Europe.

- Lenz (1934) —Europe.

- Mayer (1934a) —Europe.

- Kettle & Lawson (1952) —British.

- Gutsevich & Glukhova (1970) —former USSR

- Glukhova (1989) — Russia.

- Dzhafarov (1964) —Transcaucasus.

- Brodskaya (1999) —eastern Russia and northeastern China

- Howarth (1985) — Laos.

- Kettle & Elson (1976, 1980), Elson-Harris & Murray (1992) — Australia.

- Nevill (1969) —seven South African species.

- Nevill and Dyce (1994) — similis species group (Africa).

- Nevill et al. (2007) — imicola species group (Africa).

All the authors above have shown that there are significant differences between species of Culicoides , allowing for their identification at that level. These studies speak to the diverse morphology within this huge genus and provide good evidence that the pupal stage could be an important basis for further understanding the habitats utilized by the immatures. Larvae are far more conservative in their structural divergence and are challenging to identify (e.g. Murphree & Mullen 1991).

Dyce (1998) included pupal diagnoses for the subgenera and species groups of Australian Culicoides providing tentative characterizations (results were from a workshop).

Nevill et al. (2007) described the variation of some pupal features in the imicola species group and showed how pupae may provide morphological evidence of differences that is more obscure in adults of some species of Culicoides . Geographic variation of pupal features was described by Atchley (1971a) for three Nearctic species and sexual differences were noted in the shape of the dorsal apotome by Atchley (1971b). Spătaru (1971) described intraspecific variation of various pupal features of C. stigma .

Of the numerous features that vary between species and which were noted or utilized by previous authors, it is worth noting that the relative arrangement of sensilla D-4-I, D-8-I and D-9-I varies considerably within Culicoides , with many species having D-8-I and D-9-I lateral to D-4-I.

The diagnosis for pupae of Culicoides as given above is generally more simple than may be initially apparent. The combination of a well-developed prothoracic extension and the halter and hind leg slightly separated or barely touching distinguishes all Culicoides except for the Holarctic and rarely collected Ceratopogon , which have a unique dome-like protuberance on their dorsal apotome, and Paradasyhelea , restricted to the Southern Hemisphere ( New Zealand, Australia, New Caledonia, Argentina, Chile) and the Olympic Peninsula of Washington, USA (the latter rare) and which have a lateral row of stout, pointed spicules and further stout spicules more medially on the dorsal apotome.

The identification of the larva and pupa of C. punctatus and C. nipponensis respectively in Table 2 from Kitaoka (1998) was provided by Shigeo Kitaoka (pers. comm.).

MATERIAL EXAMINED: C. annettae : 1 pupal exuviae, 2 km NE Tarcoles, Costa Rica, 17-XII-1993 (CNCI). C. annuliductus : 1 pupal exuviae (paratype), Bayano field station, Panama Province, Panama, VI 1976 (USNM). C. arboricola : 1 pupal exuviae (paratype), Gwynns Falls Park, Baltimore, Maryland, USA, VII-1931 (USNM). C. baueri : 1 pupal exuviae, Tom’s Creek, Montgomery County, Virginia, USA, 27-V-1976 (VPIC); 1 pupal exuviae, Cedar Run, Montgomery County, Virginia, USA, 6-IX-1971 (VPIC). C. bayano : 1 pupal exuviae (paratype), Bayano field station, Panama Province, Panama, VI 1976 (USNM). C. bergi : 1 pupal exuviae (paratype), Ringwood Game Preserve, Tompkins County, New York, USA, 10-VII-1970 (USNM). C. bermudensis : 1 pupal exuviae, Hacks Neck, Acomack County, Virginia, USA, 31-VII-1976 (VPIC). C. bickleyi : 1 pupal exuviae (of holotype), Cranesville Swamp, Garrett County, Maryland, USA, 6-V-1960 (USNM). C. brookmani : 1 pupal exuviae (paratype), Arroyo Seco R.S., Monterey County, California, USA, 1-VII-1948 (USNM). C. californiensis : 1 pupal exuviae (paratype), Bakersfield Kern County, California, USA, V-1954 (USNM). C. chaverrii : 13 pupal exuviae (of holotype, paratypes), Costa Rica, various localities, dates as recorded by Spinelli and Borkent (2004) , (CNCI, INBC). C. crepuscularis : 1 pupal exuviae, Pondapas Road, Montgomery County, Virginia, USA, 3-IX- 1976 (VPIC). C. defoliarti : 1 pupal exuviae (paratype), Southwestern Research Station, Portal, Arizona, USA, 5-9- VI-1972 (USNM). C. denningi : 1 pupal exuviae (paratype), Saskatoon, Saskatchewan, Canada, VIII-1947 (USNM). C. denticulatus : 24 pupal exuviae (in glycerin), Spanish Lake, 6 km E of Falkland, 50°29.12N 119°28.07W, BC, Canada, 27–28-V-2008 (CNCI). C. dicrourus : 2 pupal exuviae, Florida, Siquirres, Limon, Costa Rica, 12-III-2006 ( INBC). C. filiductus : 1 pupal exuviae (paratype), Bayano field station, Panama Province, Panama, VI 1976 (USNM). C. guttipennis : 4 pupal exuviae, Ottawa, Ontario, Canada, 1973 (CNCI); 1 pupal exuviae, lab colony, W. Knausenberger, 30-V-1975 (VPIC). C. haematopotus : 1 pupal exuviae, 10 km W of Old Chelsea, Quebec, Canada, 15-VII-1986 (CNCI). C. heliconiae : 2 pupal exuviae, Florida, Siquirres, Limon, Costa Rica, 12-III-2006 ( INBC). C. jacksoni : 1 pupal exuviae (paratype), Cedar Creek Canyon, Lincoln County, New Mexico, USA, 13-VI-1968 (USNM). C. jamnbacki : 1 pupal exuviae (of holotype), Huntinton Marsh, Newcomb, New York, 14-V-1959 (USNM). C. kettlei : 1 pupal exuviae (paratype), Big Horn Drive, Riverside County, California, USA, 22-IX-1988 (USNM). C. loisae : 1 pupal exuviae, 10 km W of Old Chelsea, Quebec, Canada, 15- VIII-1986 (CNCI). C. neofagineus : 1 pupal exuviae (paratype), Pinery Canyon, Chiricahua Mountains, Cochise County, Arizona, USA, 10-VII-1958 (USNM). C. nubeculosus : 15 pupae, 20 pupal exuviae, from colony at Institute for Animal Health, Pirbright Laboratory, Great Britain. C. phlebotomus : 8 pupal exuviae, 3 km E of Cahuita, Costa Rica, 30-X-1993 (CNCI). C. piliferus : 1 pupal exuviae, Elliot Knob, Augusta County, West Virginia, USA, 5-VI-1977 (VPIC); 1 pupal exuviae, Little Stoney Creek, Giles County, Virginia, USA, 3-VII-1977 (VPIC). C. scanloni : 1 pupal exuviae (of holotype), Alexandria, Virginia, USA, 2-VI-1951 (USNM). C. sonorensis : 10 pupae, 10 pupal exuviae, from colony at Laramie, Wyomying, USA (CNCI). C. spinosus : 1 pupal exuviae (paratype), Roland Park, Baltimore, Maryland, USA, V-1930 (USNM). C. stellifer : 1 pupal exuviae, Watoga State Park, Pocahontas County, Virginia, USA, 1976 (VPIC). C. variipennis : 4 pupal exuviae, nr. Alfred, Ontario, Canada, 30-IV-1985 (CNCI). C. nr. crepuscularis : 3 pupal exuviae, Ohanapecosh campground turnoff, Ranier National Park, Washington, USA, 13-VI-2008 (CNCI); 1 pupal exuviae, 9 km W of Okanogan, Washington, USA, 13-VI-2008 (CNCI). C. sp.: 1 pupal exuviae, Salmon Arm, British Columbia, Canada, 7-VI-1988 (CNCI); 1 pupal exuviae, 3 km E of Salmon Arm, British Columbia, Canada, 9-VI-1988 (CNCI); 1 pupal exuviae (in glycerin), 3 km E. Carp, Ontario, Canada, 9-VI-1986 (CNCI); 10 pupal exuviae, 17 km N of Sedona, Arizona, USA, 11-V-1987 (CNCI); 4 pupal exuviae, 20 km NE of Tuscon, Arizona, USA, 4-V-1987 (CNCI); 1 pupal exuviae, Res. Sta., Stream, Newcomb, New York, USA, 6-VI-1958 (NYSM); 2 pupal exuviae, Pleasant Lake, Pierce County, North Dakota, USA, VI-1969 (USNM); 3 pupal exuviae, Iquitos plantation, Loreto, Peru, 1-II-2003 (CNCI); 5 pupal exuviae, Chittering Road, Bindoon, Western Australia, Australia, 27-X-1985 (ANIC); 34 pupal exuviae, Bindoon, Western Australia, Australia, 27-X-1985 (ANIC); 16 pupal exuviae, Bindoon (as Bundoon), Australia, 27-X (ANIC); 11 pupal exuviae, Darban, Western Australia, Australia, 28-X-1985 (ANIC); 5 pupal exuviae, as previous locality, 29-X-1985 (ANIC); 3 pupal exuviae, 5 km W of Darban, Western Australia, Australia, 29-X-1985 (ANIC); 1 pupal exuviae, Collie Road, W. Darban, Western Australia, Australia (ANIC); 1 pupal exuviae, Gap Creek, tributary of Fitzroy River, Kimberley, Western Australia, Australia (ANIC); 4 pupal exuviae, Lady Carrington Drive, Royal National Park, New South Wales, Australia (ANIC); 1 pupal exuviae, Careel Bay, New South Wales, Australia, 20-IX-1966 (ANIC); 1 pupal exuviae, no locality, 9-VI-1971 (ANIC).

Figures

FIGURE 2. Pupae in unusual habitats, preservation and relative sizes. A. Forcipomyia pupae, Rancho Grande, Venezuela; photo by Steve Marshall. B. Forcipomyia pupae under bark of log of Pinus sylvestris, Poland; photo by Marek W. Kozlowski. C. Pupae of Mallochohelea sp. on emergent plants at edge of Bolean Lk., 6 km NE Falkland, British Columbia. D. Palpomyia sp. showing mounting technique on pin, 8 km E. Sicamous, British Columbia. E. Permanent slide mount of dissected adult and pupal exuviae of Mallochohelea albibasis. F. Pupal exuviae, from left to right, of Baeodasymyia michaeli, Culicoides denticulatus and Sphaeromias longipennis showing size differences within the family. Total length of Baeodasymyia michaeli = 1.2 mm, of Sphaeromias = 7.3 mm.

FIGURE 3. Habitus of pupae of Culicoides sonorensis (from Borkent 2012). A. Female, in dorsal view. B. Male, in lateral view. C. Female, in ventral view. A and C have the abdominal segments separated by expanded membrane, not shown in B. Shagreen not shown.

FIGURE 4. Chaetotaxy of cephalothoraces of Culicoides sonorensis (modified from Borkent 2012). A. Dorsal view. B. Ventral view. C. Lateral view. Shagreen not shown.

FIGURE 5. Chaetotaxy of abdominal segment 4 of Culicoides. A. Culicoides haematopotus, in dorsal and ventral view (modified from Borkent 2012). B. Culicoides arboricola, in lateral view (from Linley 1970b).

FIGURE 13. Anterior portion of heads and thoraces, in anterior or anterodorsal view. A. Leptoconops kerteszi, ecdysial sutures of head enhanced to show position. B. Culicoides denticulatus. C. Ceratopogon nr. abstrusus. D. Brachypogon sp. (from 6 km E. Falkland, BC, Canada). E. Alluaudomyia bella, dorsal apotome absent. F. Clinohelea curriei. G. Pellucidomyia leei. H. Mallochohelea caudellii. I. Bezzia sp. (from Bolean Lake, BC, Canada).

FIGURE 15. Anterior portion of heads. A. Culicoides denticulatus, in anteroventral view. B. Ceratopogon nr. abstrusus, in anterior view. C. Brachypogon sp., in anterior view (from 6 km E. Falkland, BC, Canada). D. Stilobezzia antennalis, in ventral view, dorsal apotome not present. E. Allohelea japonica, in ventral view, dorsal apotome not present (distorted slide specimen). F. Atyphohelea macroneura, in ventral view, right side of head, dorsal apotome not present.

FIGURE 19. Dorsal apotomes, anterior view. A. Culicoides circumscriptus (from Kettle & Lawson 1952). B. Culicoides cubitalis (from Kettle & Lawson 1952). C. Culicoides truncorum (from Kettle & Lawson 1952). D. Culicoides chiopterus (from Jamnback 1965). E. Paradasyhelea minuta (from Kettle & Elson 1975a). F. Paradasyhelea albipunctata (from Elson- Harris & Kettle 1985a). G. Paradasyhelea reyei (from Elson-Harris & Kettle 1985a). H. Ceratopogon boomerangus (from Borkent & Grogan 1995). I. Ceratopogon abstrusus (from Borkent & Grogan 1995). J. Ceratopogon arcanus (from Borkent & Grogan 1995). K. Brachypogon artemis (from Debenham 1991). L. Alluaudomyia appendiculata (from Elson-Harris & Kettle 1985b). M. Alluaudomyia fumosipennis (from Elson-Harris & Kettle 1985b). N. Baeodasymyia michaeli (from Borkent & Craig 1999). O. Austrohelea campbellensis. P. Stilobezzia rabelloi (from Borkent & Craig 2001).

FIGURE 24. Posterior portion of heads, in ventral view. A. Culicoides guttipennis. B. Paradasyhelea albipunctata. C. Ceratopogon arcanus. D. Brachypogon sp. (Flag Glade, Pocahontas Co., West Virginia, USA). E. Alluaudomyia needhami. F. Baeodasymyia michaeli. G. Austrohelea campbellensis.

FIGURE 29. Dorsal setae from left side of thoraces. A. Austroconops mcmillani. B. Leptoconops kerteszi. C. Leptoconops linleyi. D. Forcipomyia (Euprojoannisia) sp. (from Peru). E. Forcipomyia (Forcipomyia) bipunctata. F. Forcipomyia (Phytohelea) n. sp. nr. antiguensis. G. Atrichopogon sp. (from Lake Opinicon, Ontario, Canada). H. Dasyhelea paracincta. I. Dasyhelea atlantis. J. Dasyhelea pseudoincisurata. K. Culicoides haematopotus. L. Culicoides phlebotomus. M. Paradasyhelea albipunctata. N. Ceratopogon boomerangus. O. Brachypogon sp. (from 6 km E. Falkland, BC, Canada). P. Alluaudomyia needhami. Q. Baeodasymyia christopheri (from Borkent & Craig 1999). R. Austrohelea campbellensis. S. Stilobezzia antennalis. T. Schizonyxhelea forattinii (from Borkent 2000a).

FIGURE 32. Cephalothoraces and abdominal segments 1–3, in lateral view. A. Austroconops mcmillani. B. Leptoconops linleyi. C. Forcipomyia (Phytohelea) sp. (Florida, USA). D. Atrichopogon sp. (from 6.5 km NW Enderby, BC, Canada). E. Dasyhelea sp., in anteroventral view (Herman Lake, 4 km SE Eagle Bay, BC, Canada). F. Dasyhelea oppresa. G. Culicoides denticulatus. H. Ceratopogon nr. abstrusus. I. Brachypogon sp. (from 6 km E. Falkland, BC, Canada). J. Alluaudomyia bella. K. Baeodasymyia michaeli. L. Stilobezzia antennalis.

FIGURE 34. Legs, wings and apices of the antennae, in ventral view. A. Austroconops mcmillani. B. Leptoconops kerteszi. C. Forcipomyia (Euprojoannisia) sp. (from Peru). D. Atrichopogon sp. (from Lake Opinicon, Ontario, Canada). E. Dasyhelea paracincta. F. Culicoides sp. (from 3 km E. Carp, Ontario, Canada).

FIGURE 43. Respiratory organs, most in dorsal view, Fig. 43T in lateral view, pattern on tracheal tubes shown only in some. A. Dasyhelea pseudoincisurata (from Waugh & Wirth 1976). B. Dasyhelea grisea (from Waugh & Wirth 1976). C. Dasyhelea traverae (from Waugh & Wirth 1976). D. Dasyhelea pseudocincta (from Waugh & Wirth 1976). E. Dasyhelea leptobranchia (from Waugh & Wirth 1976). F. Dasyhelea brevicornis (from Waugh & Wirth 1976). G. Dasyhelea hitchcocki (from Wirth 1976a). H. Culicoides chiopterus (from Jamnback 1965). I. Culicoides furens (from Jamnback 1965). J. Culicoides guttipennis (from Jamnback 1965). K. Culicoides dewulfi (from Kettle & Lawson 1952, as C. pseudochiopterus). L. Culicoides punctatus (from Kettle & Lawson 1952). M. Culicoides sanguisuga (from Jamnback 1965). N. Culicoides variipennis (from Jamnback 1965). O. Paradasyhelea albipunctata (from Elson-Harris & Kettle 1985a). P. Ceratopogon inverecundus (from Borkent & Grogan 1995). Q. Ceratopogon willisi (from Borkent & Grogan 1995). R. Brachypogon sp. (from Virginia, USA). S. Alluaudomyia needhami (from Wirth & Grogan 1981). T. Alluaudomyia fumosipennis (from Debenham 1971).

FIGURE 44. Respiratory organs, in dorsal view, pattern on tracheal tubes shown only in some. A. Alluaudomyia latipennis (from Debenham 1971). B. Alluaudomyia footei (from Wirth & Grogan 1981). C. Baeodasymyia christopheri (from Borkent & Craig 1999). D. Austrohelea campbellensis. E. Stilobezzia antennalis (from Wirth & Grogan 1981, modified). F. Stilobezzia glauca (from Wirth & Grogan 1981). G. Stilobezzia ochracea (from Kettle & Lawson 1952). H. Stilobezzia diversa (from Wirth & Grogan 1981). I. Stilobezzia rabelloi (from Borkent & Craig 2001). J. Stilobezzia navaiae (from Wirth & Grogan 1981). K. Stilobezzia lutea (from Wirth & Grogan 1981). L. Schizonyxhelea bulla (from Wirth & Grogan 1981, as a Stilobezzia). M. Schizonyxhelea forattinii (from Borkent 2000a). N. Serromyia femorata (from Kettle & Lawson 1952). O. Allohelea japonica. P.Monohelea hirsuta (from Wirth & Grogan 1981, modified). Q. Atyphohelea macroneura (from Borkent 1998). R. Parabezzia alexanderi (from Grogan & Wirth 1977a). S. Parabezzia huberti (from Grogan & Wirth 1977a). T. Echinohelea lanei (from Wirth 1994b).

FIGURE 48. Metathoraces and tergites 1, in dorsal view. A. Culicoides haematopotus. B. Paradasyhelea minuta. C. Ceratopogon sp. nr. abstrusus. D. Brachypogon sp. (from 6 km E. Falkland, BC, Canada). E. Alluaudomyia needhami. F. Baeodasymyia michaeli.

FIGURE 57. Abdominal segments four, in dorsal and ventral view (shagreen not shown). A. Culicoides haematopotus (from Borkent 2012). B. Paradasyhelea albipunctata. C. Ceratopogon boomerangus (from Borkent & Grogan 1995, compressed dorsoventrally).

FIGURE 73. Abdominal segments 9. A. Dasyhelea laeta, female, in ventral view (from Mayer 1934c). B. Dasyhelea assimilis, male, in lateral view with ventral to the right (from Mayer 1934c). C. Dasyhelea assimilis, male, in lateral view with ventral to the right (from Mayer 1934c). D. Dasyhelea grisea, male, in dorsal view (from Waugh & Wirth 1976). E. Dasyhelea chani, female, in dorsal view (from Wirth & Linley 1990). F. Dasyhelea atlantis, female, in ventral view (from Waugh & Wirth 1976). G. Dasyhelea gluchovae, female, in ventral view (from Brodskaya 1996). H. Culicoides haematopotus, female, in dorsal and ventral view (shagreen not shown). I. Paradasyhelea albipunctata, female, in dorsal view (Elson-Harris & Kettle 1985a). J. Ceratopogon boomerangus, female, in ventral view (modified from Borkent & Grogan 1995). K. Brachypogon artemis, female, in dorsal view (from Debenham 1991). L. Alluaudomyia appendiculata, female, in dorsal view (from Elson-Harris & Kettle 1985b).

FIGURE 79. Evolution of ecdysial sutures and splits in pupal exuviae of Ceratopogonidae, head and anterior portion of thorax in ventral view. Numbers refer to character states of characters 2 and 8 in text. Red indicates ecdysial splits. A. Leptoconopinae. B. Forcipomyiinae. C. Dasyheleinae. D. Most Ceratopogonini. E. Most Ceratopogonini, Clinohelea. F. Allohelea, Atyphohelea, Parabezzia. G. Heteromyia, Pellucidomyia, Hebetula. H. most Sphaeromiini s. lat., most Palpomyiini, Paryphoconus; some Bezzia are nearly completed fused (as in Fig. 79I), with only the dorsal apotome separate, along with an ecdysial split along the base of the antenna and the dorsal thoracic split. I. Jenkinshelea, Macropeza, Mallochohelea, Probezzia, Neobezzia.