Nilobezzia Kieffer

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 : 88-90

Nilobezzia Kieffer

( Figs. 21H–I , 27D , 30Q , 33H , 39C , 45O–P , 52B , 67A , 76G )

DIAGNOSIS: Only pupa of Ceratopogonidae with the metathorax with only one campaniform sensillum (M-3-T) situated at least ⅓ the length of the metathorax from its anterior margin ( Fig. 52B ), thorax with D-5-T a peg-like seta (as in Fig. 30P ) (or a short, stout seta, only in N. curticornis , then on a well-developed tubercle, Fig. 30Q ), and abdominal segment 1 with D-2-I and D-3-I closely approximated ( Fig. 52B ).

DESCRIPTION: Total length = 3.22–7.16 mm. Without larval exuviae retained on abdomen. Exuviae with flagellum appressed against lateral margin of midleg, wing (as in Figs. 16B , 33H ). Ecdysial tear around base of antenna, along lateral margin of face to palpus (as in Figs. 17C , 79H ). Head: Dorsal apotome ( Figs. 21H–I ), with ventral line of weakness, without dorsomedial tubercle, without central dome; dorsolateral cephalic sclerite (as in Fig. 13H ) fused to scutum, each side separated medially by dorsal apotome in whole pupa; mouthparts ( Fig. 27D ) with mandible well-developed, lacinia absent; palpus extending posterior to posterolateral margin of labium; labium separated medially by labrum, hypopharynx; apex of antenna ( Fig. 39C ) anterior to posterior extent of midlength portion of midleg (portion lateral to mesosternum), narrowed posteriorly; sensilla: dorsal apotomals ( Figs. 21H–I )—1 elongate seta, 1 campaniform sensillum; dorsolateral cephalic sclerite sensilla—1 seta, 1 campaniform sensillum; clypeal-labrals ( Fig. 27D )—0–1 slender or 2 thick setae; oculars ( Fig. 27D )—2 setae, 1 campaniform sensillum. Thorax: Prothoracic extension ( Fig. 27D ) wide, well-developed but narrow dorsolaterally, extending from palpus to antenna; mesonotum with very short tubercles, not extending posteromedially, not dividing metathorax medially ( Fig. 52B ); respiratory organ ( Figs. 45O–P ) length/width = 2.61–3.56, elongate, moderately slender, somewhat flattened apically, with pores closely abutting at apex of respiratory organ, arranged in single row, outer surface with a few to numbers of wrinkles, with short, wide pedicel, base with short posteromedial apodeme, membranous base of respiratory organ moderately elongate, annulated, tracheal tube straight to slightly curved along length, with spirals restricted to base, wrinkles to half length; wing ( Fig. 39C ) without apical tubercle or angle, separated medially by fore-, midlegs; halter apex and hind leg ( Fig. 33H ) broadly abutting; halter apex abutting anterolateral knob-like extension of tergite 2 or past tergite 2; legs ( Fig. 39C ) with lateral margin of foreleg near midlength of wing evenly curved; hind leg visible at lateral margin of wing ( Fig. 33H ); with apex of foreleg moderately anterior to apex of midleg; apex of hind leg abutting apex of midleg laterally; sensilla: anteromedials—1 short peg, 1 elongate seta (as in Fig. 31N ); anterolaterals—1 moderately long seta; dorsal setae ( Fig. 30Q )—D-1-T, D-2-T peg-like or setae, D-4-T seta, D-5-T peg-like seta, D-3-T campaniform sensillum, D-3-T lateral to slightly posterolateral to D-4-T; supraalar 2—campaniform sensillum; metathoracics ( Fig. 52B )—1 campaniform sensillum; M-3-T distant from margin of metathorax (at least 1/3 length of metathorax). Abdomen: pigmentation light to dark brown, with tergite 1 with 3 medial spots, tergites 2–7 with medial area with stripe, 2 anterolateral spots, 2 pairs on tergite 8 in some, sternites not pigmented or sternites 3–4 or sternites 3–7 (5–7 membranous and with single medial spot), 2 spots on sternite 8 in some, segment 2 as wide or slightly wider than segment 3, segments with undivided, thin to thick setae, with rounded to pointed, short to moderately elongate tubercles, tergites or sternites entire, not membranous or with sternites 5–7 each with membranous disc; segment 9 ( Fig. 76G ) not strongly modified, terminal processes closely approximated basally, each projecting posterodorsolaterally, tapering to pointed apex; apex of male genital lobe anterior or to level of base of terminal process (as in Figs. 78I–J ), except for N. schwarzii where it extends to about half length of base of terminal process (as in Fig. 78E ); sensilla: tergite 1 ( Fig. 52B ) with 8 setae, 2 campaniform sensilla, including 4 lateral sensilla, D-2-I, D-3-I closely approximated, D-7-I situated anterolaterally near L-1-I; segment 4 ( Fig. 67A )—D-2-IV, D-3-IV short to moderately elongate setae on short tubercles; D-5-IV, D-8-IV, D-9-IV short to moderately elongate setae; D-5-IV on single tubercle, D-8-IV, D-9-IV on separate but closely approximated tubercles, posterior dorsal sensilla in transverse row, arranged medially to laterally: D-5-IV, D-4-IV, D-8-IV, D-9- IV; D-7-IV, if present, near D-3-IV; L-1-IV short seta on rounded tubercle, near L-3-IV; L-2-IV, L-3-IV, L-4-IV short setae on pointed tubercles, V-5-IV, V-6-IV, V-7-IV short setae on short tubercles, all closely approximated; segment 8 without D-3-VIII, without L-1-VIII; segment 9 ( Fig. 76G )—with D-5-IX, D-6-IX campaniform sensilla.

DISTRIBUTION AND HABITAT: The genus Nilobezzia is known from 74 species from every Region worldwide ( Borkent 2014 ; additional species below). Immatures are present in lakes, grassy wetlands, ponds, salt marshes ( Knausenberger 1987), reservoirs, creeks, and rivers.

TAXONOMIC DISCUSSION: There are 17 species of Nilobezzia known as pupae ( Tables 2–3 ). Only two species, N. schwarzii and N. mallochi , have abdominal membranous discs (see character 50). Nearly all male pupae have short genital lobes, not extending posteriorly past the base of the terminal processes, reflecting the short, modified male adult genitalia; only those of N. schwarzii have more elongate genital lobes (even though the male adult genitalia doesn't seem disproportionally longer).

Nilobezzia theileri (de Meillon & Wirth) was originally described as a Sphaeromias ( de Meillon & Wirth 1981) but is here considered a member of Nilobezzia as a new combination as follows:

Nilobezzia theileri (de Meillon & Wirth), 1981:552 ( Sphaeromias ). new combination.

The pupa has the diagnostic features of this genus and reexamination of the adult holotype shows that the basal tooth of the claws of the adult female are actually outer and not inner, as described and inaccurately illustrated by de Meillon & Wirth (1981). The adult actually keys to Nilobezzia in the key to the Afrotropical fauna by de Meillon & Wirth (1991).

Elson-Harris (1987) keyed the pupae of six Australian species. Elson-Harris (1990) used the position of L-3-IV ventral to L-1-IV (her lpm ii "in line with" lasm) to distinguish Australian Nilobezzia from Australian Hebetula and Lanatomyia and this feature does indeed work for known Australian taxa.

MATERIAL EXAMINED: N. aranea : 1 pupal exuviae (of holotype), 1 pupal exuviae (of allotype), Breakfast Creek, Spencer, New South Wales, Australia, 4-II-1965 (ANIC); 1 pupal exuviae (of paratype), as previous locality, 3-III-1969 (ANIC); 1 pupal exuviae, McCarrs Creek, New South Wales, Australia, 22-I-1969 (ANIC); 1 pupal exuviae, Oystershell Road, New South Wales, Australia, 4-II-1965 (ANIC). N. basispinigera : 1 pupal exuviae, Warregor, Engonia, New South Wales, Australia, 11-XII-1963 (ANIC). N. brevicornis : 1 pupal exuviae, Ft. Summer #1, DeBaca County, New Mexico, USA, 21-VIII-1967 (USNM); 2 pupal exuviae, Bitter Lakes, Chaues County, New Mexico, USA, 17-VIII-1967 (USNM). N. curticornis (as N. triquetrinotata ): 1 pupal exuviae (of holotype of N. triquetrinotata ), Griffith, New South Wales, Australia, 15-XI-1956 (ANIC); 1 pupal exuviae (of allotype of N. triquetrinotata ), 6 pupal exuviae (of paratypes of N. triquetrinotata ), previous locality (ANIC). N. formosa : 1 pupal exuviae, Kozennyi Torets river, Raigorodok, Donetsk Province, Ukraine, 19–30-V-1970 (ZIN); 2 pupal, as previous locality, 1-IV-1970 (ZIN). N. fuscitarsus : 1 pupal exuviae, Darban, Western Australia, Australia, 28-X-1985 (ANIC); 2 pupal exuviae, Humpty Doo, Northern Territory, Australia, 5-XII-1958 (ANIC). N. neotropica : 1 pupal exuviae, Lago Monte Aleque, Sao Paulo State, Brazil, 5-VII-2000 (CNCI). N. robusta : 1 pupal exuviae; Douglas, Cape Province, South Africa, 23-I-1974 (NMSA); 1 pupal exuviae (of paratype), Berg River, Piquetberg, South Africa, 16-III-1953 (SAIM). N. schwarzii : 3 pupal exuviae, Lake Providence, Louisiana, USA, VII-1953 (USNM); 3 pupal exuviae, Sanibel Island, Lee County, Florida, USA, 11-V-1973 (USNM); 1 pupal exuviae, Lake Munson, Leon County, Florida, USA, 17-VIII-1987 ( JHEC); 1 pupal exuviae, 3 km N of Caldera, Costa Rica, 17-XII-1993 (CNCI). N. theileri : 1 pupal exuviae (of holotype; with adult female), Loutpan, Transvaal, South Africa, 10-I-1974 (NMSA). N. virago : 2 pupal exuviae, Darwin, Northern Territory, Australia, 7-VI-1958 (ANIC); 1 pupal exuviae, 1 pupal exuviae (of allotype), Gove, Northern Territory, Australia, II-1970 (ANIC). N. whartoni : 1 pupal exuviae, Spencer, New South Wales, Australia, 4-II-1965 (ANIC); 8 pupal exuviae, Breakfast Creek, Spencer, New South Wales, Australia, 4-II-1965 (ANIC); 1 pupal exuviae, Oystershell Road., New South Wales, Australia, 4-II-1965 (ANIC). N. sp.: 1 pupal exuviae, Constance Bay, Ontario, Canada, 8-VI-1979 (CNCI); 1 pupal exuviae (in glycerin), Kruger National Park, South Africa (ANIC); 9 pupal exuviae, Bindoon, Western Australia, Australia, 27-X-1985 (ANIC).

Figures

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 16. Anterior portion of heads. A. Parabezzia huberti, in ventral view (distorted slide specimen). B. Parabezzia sp. (5 km. E. Danby, Vermont, USA), ventrolateral view. C. Clinohelea curriei, in ventral view. D. Heteromyia clavata, in ventral view, dorsal apotome not present. E. Heteromyia wokei, in ventral, slightly lateral view. F. Pellucidomyia leei, in ventral view, dorsal apotome not present.

FIGURE 17. Anterior portion of heads. A. Jenkinshelea sp., in ventral view (from Ottawa, ON, Canada). B. Mallochohelea caudellii., in ventral view. C. Sphaeromias longipennis, in ventral view. D. Bezzia sp., in ventral view (6 km E Salmon Arm, BC, Canada). E. Palpomyia sp. (Black Lake, Quebec, Canada), in ventral view. F. Phaenobezzia sp., in ventral view (from Skulsuza, South Africa).

FIGURE 21. Dorsal apotomes, anterior view. A. Dibezzia prominens (from Mayer 1934c). B. Hebetula tonnoiri (from Elson- Harris 1987). C. Jenkinshelea albaria (from Wirth & Grogan 1979). D. Macropeza albitarsis (from Szadziewski & Dominiak, 2007). E. Mallochohelea termophila (from Spinelli 1984, modified). F. Probezzia pallida (from Wirth & Grogan 1979). G. Neobezzia fittkaui (from Ronderos et al. 2011, modified). H. Nilobezzia basispinigera (from Elson-Harris 1987). I. Nilobezzia virago (from Elson-Harris 1987). J. Johannsenomyia argentata (from Wirth & Grogan 1979). K. Lanatomyia electra (from Elson-Harris 1987). L. Anebomyia atripes (from Wirth & Grogan 1979, modified).

FIGURE 27. Posterior portion of heads, in ventral view. A. Mallochohelea caudellii. B. Probezzia sabroskyi. C. Neobezzia fittkaui. D. Nilobezzia curticornis. E. Johannsenomyia argentata. F. Lanatomyia electra. G. Anebomyia atripes. H. Homohelea delanoe.

FIGURE 30. Dorsal setae from left side of thoraces. A. Serromyia sp. B. Allohelea japonica. C. Monohelea obscura. D. Atyphohelea macroneura. E. Parabezzia huberti. F. Echinohelea lanei. G. Clinohelea curriei. H. Heteromyia clavata. I. Pellucidomyia leei. J. Dibezzia debenhamae (dirty specimen, D-5-T perhaps broken setal socket). K. Hebetula tonnoiri. L. Jenkinshelea magnipennis. M. Macropeza natalensis. N. Mallochohelea caudellii. O. Probezzia sabroskyi. P. Neobezzia fittkaui (from Ronderos et al. 2011, modified). Q. Nilobezzia curticornis. R. Johannsenomyia argentata. S. Lanatomyia miles. T. Anebomyia atripes.

FIGURE 31. Dorsal setae from left side of thoraces; anteromedial setae. A. Homohelea delanoe. B. Leehelea hispida. C. Sphaeromias longipennis. D. Xenohelea galatea. E. Bezzia nobilis. F. Clastrieromyia dycei. G. Pachyhelea pachymera. H. Palpomyia jonesi. I. Phaenobezzia mashonensis. J. Paryphoconus oliveirai. K. Echinohelea lanei, partial lateral view (distorted slide specimen). L. Palpomyia (JAD685), dorsal view. M. Palpomyia (JAD685), dorsolateral view. N. Probezzia seminigra, dorsal view of left side.

FIGURE 33. Cephalothoraces and abdominal segments 1–3, in lateral view. A. Parabezzia sp. (5 km. E. Danby, Vermont, USA). B. Clinohelea curriei. C. Pellucidomyia leei. D. Hebetula tonnoiri. E. Jenkinshelea sp. (from Ottawa, ON, Canada). F. Mallochohelea caudellii. G. Probezzia seminigra. H. Nilobezzia sp. (from Kruger NP, South Africa). I. Sphaeromias longipennis. J. Bezzia sp. (6 km E. Salmon Arm, BC, Canada) K. Palpomyia sp. (Black Lake, Quebec, Canada). L. Phaenobezzia sp. (from Skulsuza, South Africa).

FIGURE 39. Legs, wings and apices of the antennae, in ventral view. A. Probezzia sabroskyi. B. Neobezzia fittkaui. C. Nilobezzia sp. (from Australia). D. Johannsenomyia argentata. E. Lanatomyia electra. F. Anebomyia atripes.

FIGURE 45. Respiratory organs, in dorsal view, pattern on tracheal tubes shown only in some. A. Clinohelea tasmaniensis (from Elson-Harris & Kettle 1986). B. Clinohelea bimaculata (from Wirth & Grogan 1979, modified). C. Heteromyia wokei (from Wirth & Grogan 1977). D. Heteromyia clavata (from Wirth & Grogan 1977). E. Pellucidomyia leei (from Elson-Harris & Kettle 1986). F. Pellucidomyia geari (from de Meillon & Wirth 1981). G. Dibezzia prominens (from Mayer 1934c). H. Hebetula tonnoiri (from Debenham 1974). I. Jenkinshelea albaria (from Wirth & Grogan 1979). J. Macropeza albitarsis (from Szadziewski & Dominiak, 2007). K. Mallochohelea albihalter (from Wirth & Grogan 1979). L. Probezzia pallida (from Wirth & Grogan 1979). M. Probezzia xanthogaster (from Wirth & Grogan 1979). N. Neobezzia fittkaui (from Ronderos et al. 2011). O. Nilobezzia aranea (from Elson-Harris 1987). P. Nilobezzia virago (from Elson-Harris 1987). Q. Johannsenomyia argentata (from Wirth & Grogan 1979). R. Lanatomyia electra (from Debenham 1974). S. Lanatomyia miles (from Debenham 1974). T. Anebomyia atripes (from Wirth & Grogan 1979).

FIGURE 52. Metathoraces and tergites 1, in dorsal view. A. Neobezzia fittkaui. B. Nilobezzia curticornis. C. Johannsenomyia argentata. D. Lanatomyia miles. E. Anebomyia atripes. F. Homohelea delanoe (reconstructed from distorted and dirty specimen).

FIGURE 67. Abdominal segments four, in dorsal and ventral view (shagreen not shown). A. Nilobezzia curticornis. B. Johannsenomyia argentata. C. Lanatomyia miles.

FIGURE 76. Abdominal segments 9. A. Macropeza albitarsis, male, in ventral view (modified from Szadziewski & Dominiak, 2007). B. Macropeza albitarsis, female, in ventral view (from Szadziewski & Dominiak, 2007). C. Mallochohelea termophila, male, in ventral view (from Spinelli 1984). D. Mallochohelea termophila, female, in dorsal view (from Spinelli 1984). E. Probezzia pallida, male, in dorsal and ventral view (from Wirth & Grogan 1979). F. Neobezzia fittkaui, male, in dorsal view (from Ronderos, et al. 2011). G. Nilobezzia virago, female, in dorsal view (from Elson-Harris 1987). H. Johannsenomyia argentata, male, in dorsal and ventral view (from Wirth & Grogan 1979). I. Johannsenomyia argentata, female, in dorsal and ventral view (from Wirth & Grogan 1979). J. Lanatomyia miles, female, in dorsal view (from Elson- Harris 1987). K. Anebomyia atripes, male, in dorsal and ventral view (from Wirth & Grogan 1979). L. Anebomyia atripes, female, in dorsal and ventral view (from Wirth & Grogan 1979).

FIGURE 78. Abdominal segments 9. A. Palpomyia lineata, male, in dorsal and ventral view (from Grogan & Wirth 1979). B. Palpomyia lineata, female, in dorsal and ventral view (from Grogan & Wirth 1979). C. Palpomyia jonesi, male, in dorsal and ventral view (from Grogan & Wirth 1979. D. Palpomyia jonesi, female, in dorsal and ventral view (from Grogan & Wirth 1979). E. Palpomyia belkini, male, in dorsal and ventral view (from Grogan & Wirth 1979). F. Palpomyia belkini, female, in dorsal and ventral view (from Grogan & Wirth 1979). G. Palpomyia rufa, male, in dorsal and ventral view (from Grogan & Wirth 1979). H. Palpomyia flaviceps, female, in dorsal and ventral view (from Grogan & Wirth 1979). I. Phaenobezzia vacunae, male, in ventral view (from Haeselbarth 1965). J. Phaenobezzia mashonensis, male, in ventral view (from Haeselbarth 1965). K. Phaenobezzia opaca, female, in dorsal and ventral view (from Wirth & Grogan 1982). L. Paryphoconus oliveirai, female, in dorsal view (from Ronderos et al. 2007).

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.