Culicoides Latreille
Creators: name: Borkent, Art
Publisher: name: Zenodo
Year: 2014
Subjects: Biodiversity
Taxonomy
Animalia
Arthropoda
Insecta
Diptera
Ceratopogonidae
Culicoides

description: 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).
description: Published as part of 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, pp. 1-327 in Zootaxa 3879 (1) on pages 49-51, DOI: 10.11646/zootaxa.3879.1.1, http://zenodo.org/record/4949051