Parabezzia Malloch

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 : 72-73

Parabezzia Malloch

( Figs. 16A–B , 20K–L , 25H , 30E , 33A , 37B , 44R–S , 50B , 62B–C , 74L , 75A )

DIAGNOSIS: Only pupa of Ceratopogonidae with a well-developed prothoracic extension ( Fig. 25H ) and the mesonotum with only 2 setae (D-1-T, D-2-T) and D-3-T (campaniform sensillum) ( Fig. 30E ). Also, only pupa of Ceratopogonidae with a well-developed prothoracic extension ( Fig. 25H ) and the abdominal segment 4 with 9-10 sensilla ( Figs. 62 B-C) (lacking D-3-IV, L-1-IV, L-4-IV, V-7-IV and, in some, D-9-IV).

DESCRIPTION: Total length = 1.50–2.59 mm. Without larval exuviae retained on abdomen. Exuviae with flagellum appressed against lateral margin of face, midleg, wing ( Figs. 16A–B , 33A ). Ecdysial tear medial to antennal base (as in Figs. 15D , 79D ) or tearing into eye, either posteriorly or posterolaterally ( Figs. 16A–B , 79F ). Head: Dorsal apotome ( Figs. 20K–L ), without 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. 25H ) with mandible well-developed, lacinia absent; palpus extending posterior to posterolateral margin of labium; labium entire (not divided medially); apex of antenna ( Fig. 37B ) equal to posterior to, posterior extent of midlength portion of midleg (portion lateral to mesosternum), narrowed posteriorly; sensilla: dorsal apotomals ( Figs. 20K–L )—1 short seta, 1 campaniform sensillum; dorsolateral cephalic sclerite sensilla—1 very short seta, 1 campaniform sensillum or 2 setae (only in P. petiolata ); clypeallabrals ( Fig. 25H )—absent or 1 short peg; oculars ( Fig. 25H )—1 campaniform sensillum. Thorax: Prothoracic extension ( Fig. 25H ) wide, well-developed, extending from palpus to antenna; mesonotum with or without welldeveloped moderately sized tubercles, not extending posteromedially, with or without slight protuberance, not dividing metathorax medially ( Fig. 50B ); respiratory organ ( Figs. 44R–S ) length/width = 1.95–2.82, short, squat, somewhat flattened dorsoventrally, with pores closely abutting at apex of respiratory organ, arranged in single row, outer surface with some wrinkles, with or without short, wide pedicel, base with short posteromedial apodeme, membranous base of respiratory organ short, tracheal tube straight to slightly curved along length, with annulations to half length; wing ( Fig. 37B ) with apical tubercle lateral to apex of hind leg, separated medially by fore-, midlegs; halter apex and hind leg ( Fig. 33A ) broadly abutting; halter apex abutting anterolateral knob-like extension of tergite 2; legs ( Fig. 37B ) with lateral margin of foreleg near midlength of wing with abrupt angle or evenly curved; hind leg visible at lateral margin of wing ( Fig. 33A ); with apex of foreleg slightly to moderately anterior to apex of midleg; apex of hind leg abutting apex of midleg laterally; sensilla: anteromedials—1 very short seta, 1 campaniform sensillum; anterolaterals—1 short seta; dorsal setae ( Fig. 30E )—D-1-T, D-2-T peg-like setae, D-3-T campaniform sensillum; D-2-T, D-3-T on single tubercleor closely approximated tubercles; supraalar 2—campaniform sensillum; metathoracics ( Fig. 50B )—2 campaniform sensilla; M-3-T near anterior margin of metathorax. Abdomen: with 2 spots medially on tergites 1-7 or tergites 1-3 and fading posteriorly, segment 2 as wide or slightly wider than segment 3, segments with undivided, peg-like or thin to thick setae, with rounded to pointed or apically toothed, short to moderately elongate tubercles, tergites or sternites entire, not membranous or sternites 4-7 or 4-8 each with narrow membranous disc; segment 9 ( Figs. 74L , 75A ) not strongly modified, terminal processes closely approximated basally, each projecting nearly posteriorly to posterodorsolaterally, tapering to pointed apex; sensilla: tergite 1 ( Fig. 50B ) with 5 setae, 2 campaniform sensilla or 7 setae, 2 campaniform sensilla, including 4 lateral sensilla, D-2-I present, D-3 absent, D-7-I situated anterolaterally near L- 1-I; segment 4 ( Figs. 62 B-C)—D-2-IV peg-like seta on short to moderately elongate tubercle, D-3-IV absent; D-5- IV peg-like seta, D-8-IV, D-9-IV (when present) short setae; only D-8-IV on short tubercle or D-5-IV, D-8-IV, D-9- IV on moderately elongate, separate tubercles, posterior dorsal sensilla in transverse row, arranged medially to laterally: D-5-IV, D-4-IV, D-8-IV or D-5-IV, D-4-IV, D-8-IV, D-9-IV; L-1-IV absent, L-2-IV, L-3-IV short setae on pointed or toothed tubercles, L-4-IV absent, V-5-IV, V-6-IV short setae, V-5-IV without tubercle or on short toothed tubercle, V-6-IV on short toothed or pointed tubercle,V-7-IV absent; segment 8 without D-3-VIII, without L-1-VIII; segment 9 ( Figs. 74L , 75A )—with D-5-IX, D-6-IX campaniform sensilla.

DISTRIBUTION AND HABITAT: The genus Parabezzia is known from 40 species from nearly every Region worldwide but absent from most of the Palaearctic (only in north Africa) and the Australasian Region ( Borkent 2014 ). Pupae have been collected on the edges of streams, rivers and ponds. Grogan & Wirth (1977a) reported that P. alexanderi pupae were the most common of all ceratopogonids at a lily pond in Maryland, USA.

TAXONOMIC DISCUSSION: There are seven species of Parabezzia known as pupae ( Tables 2–3 ). There are two quite different types of pupae in this genus. One has numbers of rounded tubercles ( Figs. 33A , 62B ), the other, called the alexanderi group, has sharp tubercles ( Fig. 62C ) and abdominal sternites with membranous discs (e.g. P. alexanderi , P. balseiroi ).

All species of Parabezzia have reduced numbers of sensilla on every part of the body (see diagnosis). Some species have no clypeal-labral setae ( P. bystraki , P. stagni ) while others have a single peg ( P. huberti , P. alexanderi , P. downesi , P. petiolata , P. balseiroi ), a condition unique in the family.

Grogan & Wirth (1977a) provided a key to the pupae of the four Nearctic species known at that time and Wirth & Grogan (1981) included a key to three species at Plummer's Island, Maryland, USA, including the newly described pupa of P. bystraki .

Harris (1981) and Elson-Harris (1990) described the pupa of " Ceratopogon sp. n. 1" from Australia which would fit the diagnosis and distinctive description of Parabezzia here (the reared adult was not subsequently described). The described presence of eight sensilla on abdominal segment 4 (she likely missed the small campaniform sensilla D-4-IV and D-7-IV, hence a total of 10) is unique within the Ceratopogoninae for Parabezzia . However, at present there are no Parabezzia otherwise known from the Australasian Region. One potential candidate may be Heteroceratopogon , a genus related to Parabezzia and present in Australia. Unfortunately, the original material has been lost (Marlene Elson-Harris, pers. comm. 1993).

If Harris (1981) correctly associated the larvae with the pupa and the above reidentification is correct, she provides the only larval description of a species of Parabezzia (or the only known larva and pupa of Heteroceratopogon ).

Grogan & Wirth (1977a) illustrated the dorsal apotomes of species of Parabezzia with DA-2-H being a very short seta but reexamination of original material indicates that these are campaniform sensilla, as in nearly all other Ceratopogonidae . Previous descriptions ( Table 2 ) missed D-7-IV (campaniform sensillum) on abdominal segment 4.

MATERIAL EXAMINED: P. alexanderi : 1 pupal exuviae, Lakeland Pond, College Park, Prince George’s County, Maryland, USA, 11-VI-1975 (USNM); 3 pupal exuviae, as previous locality, 27-V-1975 (2 WLGC, 1 CNCI); 2 pupal exuviae, as previous locality, 30-V-1975 (1 USNM, 1 CNCI). P. balseiroi : 2 pupal exuviae (of paratypes), Santa Ana, Entre Rios, Argentina, 9-XI-1984 (MLPA). P. bystraki : 1 pupal exuviae, Patuxent Wildlife Rescue Center, Prince George’s County, Maryland, USA, 20-VII-1976 (USNM). P. downesi : 9 pupal exuviae (of paratypes), Algonquin Park, Ontario, Canada, 8-VI-1960 (3 CNCI, 6 USNM). P. eupetiolata : 1 pupal exuviae (of paratype), 1 pupal exuviae (of allotype), Glenfield, Independence River, Lewis County, New York, USA, 22-VI- 1963 (USNM). P. huberti : 1 pupal exuviae, Patuxent Wildlife Rescue Center, Prince George’s County, Maryland, USA, 20-VII-1977 (USNM); 4 pupal exuviae (of paratypes), Falls Church, Virginia, USA, 22-VII-1951 (USNM); 2 pupal exuviae (of paratypes), Mount Solon, Virginia, 4-VII-1951 (USNM). P. stagni : 1 pupal exuviae (of holotype), Doornpan, Bulge River, North Transvaal, South Africa, 6-XI-1973 (NMSA). P. sp.: 1 pupal exuviae, 5 km E of Dandy, Vermont, USA, 25-VI-1986 (CNCI).

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 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 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 20. Dorsal apotomes, anterior view. A. Stilobezzia soror (from Mayer 1934c). B. Stilobezzia lutea (from Wirth & Grogan 1981). C. Stilobezzia antennalis (from Wirth & Grogan 1981). D. Stilobezzia pallidiventris (from Wirth & Grogan 1981). E. Schizonyxhelea forattinii (from Borkent 2000a). F. Schizonyxhelea bulla (from Wirth & Grogan 1981, modified). G. Serromyia sp.. H. Allohelea japonica. I. Monohelea obscura. J. Atyphohelea macroneura (from Borkent 1998). K. Parabezzia alexanderi male (from Grogan & Wirth 1977a, modified). L. Parabezzia alexanderi female (from Grogan & Wirth 1977a, modified). M. Clinohelea dryas (from Elson-Harris & Kettle 1986). N. Clinohelea tasmaniensis (from Elson-Harris & Kettle 1986). O. Heteromyia wokei (from Wirth & Grogan 1977, modified). P. Pellucidomyia leei (from Elson-Harris & Kettle 1986).

FIGURE 25. Posterior portion of heads, in ventral view. A. Stilobezzia antennalis. B. Stilobezzia rabelloi (from Borkent & Craig 2001). C. Schizonyxhelea bulla. D. Serromyia sp.. E. Allohelea japonica. F. Monohelea obscura (reconstructed from distorted specimen). G. Atyphohelea macroneura. H. Parabezzia huberti.

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 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 37. Legs, wings and apices of the antennae, in ventral view. A. Atyphohelea macroneura. B. Parabezzia huberti. C. Echinohelea lanei (reconstructed from distorted specimen). D. Clinohelea currei. E. Heteromyia clavata. F. Pellucidomyia leei.

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 50. Metathoraces and tergites 1, in dorsal view. A. Atyphohelea macroneura. B. Parabezzia huberti. C. Echinohelea lanei. D. Clinohelea currei. E. Heteromyia wokei. F. Pellucidomyia leei.

FIGURE 62. Abdominal segments four, in dorsal and ventral view (shagreen not shown). A. Atyphohelea macroneura (from Borkent 1998). B. Parabezzia huberti. C. Parabezzia alexanderi.

FIGURE 74. Abdominal segments 9. A. Baeodasymyia michaeli, female, in dorsal view (modified from Borkent & Craig 1999). B. Austrohelea campbellensis, female, in dorsal and ventral view (reconstructed from distorted specimen, shagreen not shown). C. Stilobezzia lutea, male, in dorsal and ventral view (from Wirth & Grogan 1981). D. Stilobezzia lutea, female, in dorsal and ventral view (from Wirth & Grogan 1981). E. Stilobezzia rabelloi, male, in ventral view (from Borkent & Craig 2001). F. Schizonyxhelea bulla, female, in dorsal and ventral view (from Wirth & Grogan 1981). G. Schizonyxhelea forattinii, female, in ventral view (from Borkent 2000a). H. Serromyia sp., female (in dorsal and ventral view (reconstructed from distorted specimen, shagreen not shown). I. Allohelea japonica, female, in dorsal and ventral view (shagreen not shown). J. Monohelea obscura, male, in dorsal and ventral view (reconstructed from distorted specimen, shagreen not shown). K. Atyphohelea macroneura, female, in dorsal view (from Borkent 1998). L. Parabezzia huberti, male, in ventral view (from Grogan & Wirth 1977a).

FIGURE 75. Abdominal segments 9. A. Parabezzia huberti, female, in ventral view (from Grogan & Wirth 1977a). B. Echinohelea lanei (from Wirth 1994b). C. Clinohelea bimaculata, female, in ventral view (from Wirth & Grogan 1979). D. Heteromyia wokei, male, in dorsal and ventral view (from Wirth & Grogan 1977). E. Heteromyia wokei, female, in dorsal and ventral view (from Wirth & Grogan 1977). F. Heteromyia clavata, female, in dorsal and ventral view (from Wirth & Grogan 1977). G. Pellucidomyia leei, male, in dorsal view (from Elson-Harris & Kettle 1986). H. Pellucidomyia geari, male, in ventral view (from de Meillon & Wirth 1981). I. Dibezzia debenhamae, male, in dorsal and ventral view (shagreen not shown). J. Hebetula tonnoiri, female, in dorsal view (from Elson-Harris 1987). K. Jenkinshelea albaria, male, in dorsal and ventral view (from Wirth & Grogan 1979). L. Jenkinshelea albaria, female, in dorsal and ventral view (from Wirth & Grogan 1979).

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.