Simulium (Gomphostilbia) asakoae Takaoka & Davies, 1995

Takaoka, Hiroyuki, Sofian-Azirun, Mohd, Ya’Cob, Zubaidah, Chen, Chee Dhang, Lau, Koon Weng, Low, Van Lun, Pham, Xuan Da & Adler, Peter H., 2017, The black flies (Diptera: Simuliidae) of Vietnam, Zootaxa 4261 (1), pp. 1-165 : 15-23

Simulium (Gomphostilbia) asakoae Takaoka & Davies, 1995

Simulium (Gomphostilbia) asakoae Takaoka & Davies, 1995: 55 –60 (Female, male, pupa and larva); Takaoka et al., 2014b: 743; Pham, 1998: 121.

Simulium (G.) asakoae was originally described from Peninsular Malaysia ( Takaoka and Davies 1995) and recorded from Vietnam ( Pham 1998). A reexaminantion shows that the following characters differ from the original description of this species: male antenna yellowish except apical five or six flagellomeres darkened, pupal abdominal segments 1 and 2 without minute tubercles, and larval labral fan with 42–48 primary rays, and length ratio of the antennal articles 1–3 (1.0:0.9–1.0:0.9–1.1). An analysis of DNA sequences shows only a slight difference between S. (G.) asakoae populations from Vietnam and those from Peninsular Malaysia (Low et al. unpublished data).

Female. Body length 2.4–2.5 mm. Head. Slightly narrower than width of thorax. Frons brownish black, densely covered with yellowish-white scale-like recumbent short hairs interspersed with few dark longer hairs near vertex; frontal ratio 1.7–1.8:1.0:2.3–2.5; frons:head ratio 1.0:4.6–5.0. Fronto-ocular area well developed, narrow, directed dorsolaterally. Clypeus brownish black, densely covered with yellowish-white scale-like hairs interspersed with several dark longer hairs on each side. Labrum 0.54–0.56 times length of clypeus. Antenna composed of scape, pedicel and nine flagellomeres, light to dark brown except scape and pedicel yellow, and base of first flagellomere yellowish white. Maxillary palp composed of five segments, light to medium brown, proportional lengths of third, fourth, and fifth segments 1.0:1.1–1.2:2.8–2.9; third segment ( Fig. 4 A, B) widened apically; sensory vesicle ( Fig. 4 A, B) small or medium sized, ellipsoidal (0.3–0.4 times length of third segment), with medium or large opening. Maxillary lacinia with 9–12 inner and 13 or 14 outer teeth. Mandible ( Fig. 4 C) with 22 or 23 inner teeth and five or six outer teeth at some distance from tip. Cibarium ( Fig. 4 D) medially forming sclerotized plate folded forward from posterior margin, with moderately sclerotized mediolongitudinal ridge with bifid apex. Thorax. Scutum dark brown except anterolateral calli ochreous, and three blackish longitudinal vittae (one median, two submedian), thinly pruinose and shiny when illuminated at certain angles, densely covered with whitish-yellow to yellow scale-like recumbent short hairs except three vittae with dark recumbent short hairs. Scutellum medium brown, covered with yellow short hairs and dark-brown long upright hairs along posterior margin. Postnotum dark brown, slightly shiny when illuminated at certain angles, and bare. Pleural membrane bare. Katepisternum longer than deep, medium to dark brown, shiny when illuminated at certain angles, moderately covered with fine short hairs. Legs. Foreleg: coxa and trochanter yellowish white; femur dark yellow with apical cap light brown (though extreme tip yellowish, and basal two-thirds of inner surface yellowish white); tibia white except apical three-tenths dark brown, and little more than basal one-fourth grayish on inner surface, and covered with white fine hairs on basal four-fifths; tarsus brownish black, with moderate dorsal hair crest; basitarsus moderately dilated, 6.0–6.4 times as long as its greatest width. Midleg: coxa medium brown except posterolateral surface dark brown; trochanter whitish yellow; femur light brown with basal one-fifth whitish yellow and apical cap medium brown (though extreme tip yellowish); tibia yellowish white on basal three-fourths to four-fifths (though apical two-thirds of anterior surface appearing darkened due to dark hair covering) and apical cap brownish black, covered with yellowish fine hairs on posterior and inner surfaces of basal two-thirds; tarsus dark brown to brownish black though basal half of basitarsus yellowish white. Hind leg: coxa light brown except apical one-third yellowish; trochanter whitish yellow; femur light brown with base whitish yellow and apical cap dark brown (though extreme tip yellowish white); tibia ( Fig. 4 E) yellowish white on basal two-thirds and brownish black on rest, covered with whitish fine hairs on outer and posterior surfaces of little more than basal three-fourths; tarsus brownish black except basal two-thirds (though base light brown) and basal half of second tarsomere yellowish white; basitarsus ( Fig. 4 F) narrow, nearly parallel-sided though slightly narrowed apically, 5.5–6.2 times as long as wide, and 0.7 and 0.6–0.7 times as wide as greatest widths of tibia and femur, respectively; calcipala ( Fig. 4 F) nearly as long as width at base, and 0.6 times as wide as greatest width of basitarsus; pedisulcus ( Fig. 4 F) well developed; claw ( Fig. 4 G) with large basal tooth 0.46–0.50 times length of claw. Wing. Length 2.0– 2.1 mm. Costa with dark spinules and hairs except basal patch of hairs yellow. Subcosta with dark hairs except near apex bare. Hair tuft on base of radius yellow. Basal portion of radius fully haired; R1 with dark spinules and hairs; R2 with hairs only. Basal cell absent. Halter . White except basal portion darkened. Abdomen. Basal scale ochreous, with fringe of whitish-yellow hairs. Dorsal surface of abdomen medium to dark brown except anterior half or little more of segment 2 whitish, moderately covered with dark short to long hairs; tergites of segments 2 and 6–9 shiny when illuminated at certain angles. Ventral surface of segment 2 white, those of segments 3 and 4 dark yellow to light brown and those of other segments medium brown; sternal plate on segment 7 undeveloped. Terminalia . Sternite 8 ( Fig. 4 H) bare medially, with 18–22 medium-long to long hairs together with four or five slender short hairs on each side. Ovipositor valve ( Fig. 4 H) triangular (though posteromedial corner rounded), thin, membranous, moderately covered with microsetae interspersed with one or two short hairs; inner margins slightly sinuous, somewhat sclerotized, and moderately separated from each other. Genital fork ( Fig. 4 I) of usual inverted- Y form, with slender stem; arms of moderate width, moderately folded medially, without lobe directed posteromedially. Paraproct in ventral view ( Fig. 4 J) somewhat concave anterolaterally, with six sensilla on anteromedial surface; paraproct in lateral view ( Fig. 4 K) slightly produced ventrally beyond ventral tip of cercus, 0.6–0.7 times as long as wide, with 22–27 medium-long to long hairs on ventral and lateral surfaces. Cercus in lateral view ( Fig. 4 K) short, rounded posteriorly, 0.4 times as long as wide. Spermatheca ( Fig. 4 L) ellipsoidal, 1.4– 1.5 times as long as its greatest width, well sclerotized except duct and small area near juncture with duct unsclerotized, and with many fissures on outer surface; internal setae absent; both accessory ducts slender, subequal in diameter to major one.

Male. Body length 2.5–2.6 mm. Head. Somewhat wider than thorax. Upper eye bright medium brown, consisting of 11 (rarely 12) vertical columns and 13 (rarely 14) horizontal rows of large facets. Face brownish black, white pruinose. Clypeus brownish black, whitish pruinose, densely covered with golden-yellow scale-like medium-long hairs (mostly directed upward) interspersed with several dark-brown simple longer hairs. Antenna composed of scape, pedicel and nine flagellomeres, yellowish except flagellomeres 5–9 light to medium brown (or yellow to dark yellow except base of flagellomere 1 yellowish white and flagellomeres 8 and 9 light to medium brown in one male); first flagellomere elongate, 1.7 times length of second one. Maxillary palp light to medium brown, with five segments, proportional lengths of third, fourth, and fifth segments 1.0:1.2–1.3:3.0–3.2; third segment ( Fig. 5 A, B) slender; sensory vesicle ( Fig. 5 A, B) small, globular or ellipsoidal (0.2 times length of third segment), and with small opening. Thorax. Scutum dark brown, with longitudinal vittae (one median, two submedian) invisible or faintly visible, shiny and thinly gray pruinose when illuminated at certain angles, and densely covered with whitish-yellow scale-like recumbent short hairs. Scutellum medium brown, covered with yellow short hairs and dark-brown long upright hairs along posterior margin. Postnotum dark brown, slightly shiny and white pruinose when illuminated at certain angles, and bare. Pleural membrane bare. Katepisternum medium to dark brown, longer than deep, shiny when illuminated at certain angles, moderately covered with fine short hairs. Legs. Foreleg: coxa whitish yellow; trochanter yellow; femur dark yellow to light brown with apical cap medium brown (though apical tip yellowish); tibia white except apical three-tenths dark brown, and covered with white hairs on white portion; tarsus brownish black; basitarsus moderately dilated, 7.1–7.4 times as long as its greatest width. Midleg: coxa light brown except posterior surface dark brown; trochanter yellowish; femur light brown with base yellowish and apical cap medium brown (though apical tip yellow); tibia medium to dark brown except basal one-third or little more whitish; tarsus dark brown except basal one-third or less of basitarsus yellow (border not well defined). Hind leg: coxa light brown except apical portion yellow; trochanter yellowish; femur medium brown with base yellowish white and apical cap dark brown (though apical tip yellow); tibia ( Fig. 5 C) dark brown to brownish black except basal three-sevenths yellowish white; tarsus ( Fig. 5 D) medium to dark brown except little less than basal half of basitarsus and basal half of second tarsomere whitish yellow; basitarsus ( Fig. 5 D) enlarged, wedge-shaped, 3.3–3.5 times as long as wide, and 1.0–1.1 and 1.1–1.3 times as wide as greatest width of tibia and femur, respectively; calcipala ( Fig. 5 D) slightly shorter than basal width, and 0.3 times as wide as greatest width of basitarsus. Pedisulcus ( Fig. 5 D) well developed. Wing. Length 2.0 mm. Other characters as in female except subcosta with one to three hairs (rarely no hairs). Halter . Dull white except basal stem darkened. Abdomen. Basal scale dark brown, with fringe of light-brown hairs. Dorsal surface of abdomen dark brown to brownish black except segment 2 light brown, covered with dark-brown short to long hairs except segment 2 with yellowish hairs; segments 2 and 5–8 each with pair of shiny dorsolateral or lateral patches; ventral surface of segment 2 whitish, those of segments 3 and 4 grayish white though sternal plates light brown, and those of other segments medium to dark brown. Genitalia. Coxite in ventral view ( Fig. 5 E) nearly rectangular, 1.7 times as long as its greatest width. Style in ventral view ( Fig. 5 E) bent inward, with triangular apex having single spine; style in ventrolateral view ( Fig. 5 F) slightly tapered toward apex, with truncated apex. Ventral plate in ventral view ( Fig. 5 E) with body transverse, 0.6 times as long as wide, with anterior margin produced anteromedially, posterior margin somewhat concave medially, and lateral margin emarginated medially, and densely covered with microsetae on ventral surface; basal arms of moderate length, slightly divergent, then convergent apically; ventral plate in lateral view ( Fig. 5 G) moderately produced ventrally; ventral plate in caudal view ( Fig. 5 H) rounded ventrally, though ventral margin nearly straight medially, densely covered with microsetae on posterior surface. Median sclerite ( Fig. 5 I) plate-like, wide. Parameres ( Fig. 5 J) of moderate size, each with four distinct long and medium-long stout hooks, and without minute setae on outer surface of basal arm. Aedeagal membrane ( Fig. 5 J) moderately setose; dorsal plate not defined. Ventral surface of abdominal segment 10 ( Fig. 5 K, L) slightly sclerotized along anterior margin and without distinct hairs near posterolateral corners. Cercus ( Fig. 5 K, L) small, rounded, with 12–17 hairs.

Pupa. Body length 2.5–2.7 mm. Head. Integument yellow, moderately covered with small round tubercles except antennal sheaths and ventral surface almost bare; antennal sheath without any protuberances; frons with three pairs of unbranched long trichomes with or without coiled apices ( Fig. 6 A); face with pair of unbranched (rarely bifid) long trichomes with straight apices ( Fig. 6 A); three frontal trichomes on each side arising close together, subequal in length to one another and slightly longer than facial one. Thorax. Integument yellow, moderately covered with round tubercles, and with three long dorsomedial trichomes of different lengths (anterior trichome longest, posterior one shortest) with coiled apices ( Fig. 6 A), two long anterolateral trichomes (anterior trichome more slender and shorter with straight apex, posterior one with coiled apex) ( Fig. 6 A), one medium-long mediolateral trichome with straight apex ( Fig. 6 A), and three ventrolateral trichomes (one medium-long, two short) with straight apices ( Fig. 6 A) on each side; all trichomes unbranched except dorsal trichomes rarely bifid. Gill ( Fig. 6 B) composed of eight slender thread-like filaments, arranged as [3+(1+2)]+2 or [(2+1)+(1+2)]+2 from dorsal to ventral, with short common basal stalk having somewhat swollen transparent basal fenestra at base; common basal stalk 0.6 times length of interspiracular trunk; dorsal and middle triplets sharing short stalk, and dorsal triplet composed of three individual filaments arising at same level, with short stalk, or composed of one individual and two paired filaments with extremely short stalk, middle triplet composed of one individual and two paired filaments and bearing short primary and secondary stalks; stalk of ventral pair of filaments medium-long, 1.4–1.7 times length of common basal stalk, and 0.8–1.0 times length of interspiracular trunk, and 0.9 times as thick as common stalk of middle and dorsal triplets; common stalk of dorsal and middle triplets shorter than primary stalk of middle triplet, and shorter or longer than stalk of dorsal triplet; middle triplet primary stalk longer than secondary stalk; primary stalk of dorsal triplet lying against that of lower pair at angle of 70–90 degrees when viewed laterally; filaments of dorsal triplet subequal in length (1.4–2.0 mm) and thickness to one another; filaments of middle triplet subequal in length (1.8–2.7 mm) and thickness to one another; two filaments of ventral pair subequal in length (2.6–3.2 mm) and thickness to each other and 1.4 and 1.3 times as thick as dorsal and middle triplets of filaments when compared basally; all filaments medium to dark brown, gradually tapered toward apex; cuticle of all filaments with well-defined annular ridges and furrows though becoming less marked apically, densely covered with minute tubercles. Abdomen ( Fig. 6 C, E). Dorsally, segments 1 and 2 and basal half or more of segment 3 (and rarely segment 4) light grayish, and other segments yellowish; all segments without tubercles; segment 1 with one unbranched slender medium-long hair-like seta on each side; segment 2 with one unbranched slender medium-long hair-like seta and five somewhat spinous minute setae submedially on each side; segments 3 and 4 each with four hooked spines and one somewhat spinous minute seta on each side; segment 5 lacking spinecombs and comb-like groups of minute spines on each side; segments 6–9 each with spine-combs in transverse row and comb-like groups of minute spines on each side (though spine-combs rarely absent on segment 9); segments 5– 8 each with few minute setae near posterior margin on each side; segment 9 with pair of wide flat terminal hooks, of which outer margin is 3.5–4.1 times length of inner margin and crenulated ( Fig. 6 D) when viewed caudally. Ventrally, segment 4 with one unbranched hook (subequal in size to those on segments 5–7) and few slender short setae on each side; segment 5 with pair of bifid hooks submedially and few short slender setae on each side; segments 6 and 7 each with pair of bifid (rarely trifid) inner and unbranched outer hooks somewhat spaced from each other and few short slender setae on each side; segments 4–8 each with comb-like groups of minute spines. Each side of segment 9 with three or four grapnel-shaped hooklets ( Fig. 6 F). Cocoon ( Fig. 6 G). Wall-pocketshaped, roughly to moderately woven, widely extended ventrolaterally; anterior margin thickly woven medially, often with buldge; posterior three-fifths with floor roughly woven; individual threads visible; 3.4–4.0 mm long by 2.0–3.0 mm wide.

Mature larva. Body length 5.0– 5.6 mm. Body light ochreous except ventral surface of abdominal segments 5– 9 whitish, with following color markings: thoracic segment 1 encircled with reddish-brown band (though disconnected ventromedially) narrowly along anterior margin, thoracic segments 2 and 3 reddish brown on ventral surface; abdominal segment 3 with or without pair of narrow reddish-brown lateral spots; abdominal segment 4 with pair of reddish-brown dorsolateral spots rarely faintly connected to each other ventrally, abdominal segments 5 and 6 each encircled by reddish-brown transverse band though disconnected ventromedially (often faded out leaving round dorsomedian spot) and three similar colored spots on ventral surface, though those on segment 6 much lighter, abdominal segments 7–9 each covered with similar colored pigments to varying extent (as transverse band similar to those on segments 5 and 6 in some larvae, but completely faded out in other larvae) on dorsal and dorsolateral surface; abdominal segment 7 with similar colored transverse band ventrally (though usually faded out in most larvae). Head. Head capsule ( Fig. 7 A–C) yellow to dark yellow except eye-spot region whitish, sparsely covered with minute setae (though moderately to densely on dorsal surface); head spots moderately positive though anterior spots of posterolateral spots usually faint or indistinct ( Fig. 7 A); eyebrow distinct with small round dark spot above it ( Fig. 7 B). Antenna composed of three articles and apical sensillum, longer than stem of labral fan; proportional lengths of first, second, and third articles 1.0:0.9–1.0:0.9–1.1. Labral fan with 42–48 primary rays. Mandible ( Fig. 7 D) with three comb-teeth decreasing in length from first tooth to third; mandibular serration composed of two teeth (one medium-sized, one small); major tooth at angle of little less than 90 degrees against mandible on apical side; supernumerary serrations absent. Hypostoma ( Fig. 7 E) with row of nine apical teeth, of which median tooth is longer than each corner tooth; lateral margin smooth; five or six hypostomal bristles per side lying nearly parallel to lateral margin. Postgenal cleft ( Fig. 7 C) arrow-head-shaped, medium-long, 2.2–2.7 times length of postgenal bridge. Cervical sclerites composed of pair of small yellow rod-like pieces. Thorax and Abdomen. Thoracic proleg without hairs; thoracic cuticle and abdominal cuticle of segments 1 and 2 sparsely covered with unbranched unpigmented minute setae on dorsal surface; abdominal cuticle of segments 3–5 sparsely covered with unbranched dark minute setae and unpigmented minute setae on dorsal surface, that of segments 6–9 moderately covered with slightly darkened unbranched minute setae mixed with unpigmented shorter minute setae ( Fig. 7 F) on dorsal and dorsolateral surfaces; last abdominal segment densely covered with unbranched colorless minute setae on dorsolateral and lateral surfaces of each side of anal sclerite and on each lateral surface even down to base of ventral papilla; thorax and abdomen without dorsal protuberances. Rectal scales absent. Rectal organ compound, each of three lobes with 9–11 finger-like secondary lobules. Anal sclerite of usual X-form, with anterior arms 1.1 times as long as posterior ones, broadly sclerotized at base; no sensilla on broad base and posterior to posterior arms; accessory sclerite absent. Last abdominal segment with pair of large conical ventral papillae. Posterior circlet with 82–85 rows of hooklets with up to 13–15 hooklets per row.

Specimens examined: Five females, five males (together with their associated pupal exuviae), reared from pupae and 10 mature larvae, collected from a slow-flowing stream (width 0.5–1.5 m, depth 10–20 cm, bottom rocky, water temperature 18.0˚C, exposed to the sun, elevation 920 m, 21˚27’501’’N/105˚38’941’’E), Tam Dao, Vinh Phuc Province, northern Vietnam, 8-XI-2013, by H. Takaoka, M. Sofian-Azirun, Z. Ya’cob, C.D. Chen & K.W. Lau; one female and one male, one pupal exuviae and one mature larva, collected from a stream (width 30 cm, depth 5 cm, bottom sandy, water temperature 18.0˚C, exposed to the sun, elevation 80 m, 19˚20’12.147”N/ 105˚09’15.908”E) slow flowing near a forest, Chau Dinh, Quy Chau, Nghe An Province, northern Vietnam, 11- XII-2015, by H. Takaoka, M. Sofian-Azirun, C.D. Chen & K.W. Lau.

Distribution. Peninsular Malaysia, Hong Kong, Thailand, Vietnam (Lam Dong, Thua Thien Hue, Nghe An and Vinh Phuc)

Remarks. Simulium (G.) asakoae is characterized in the female by the mandible with several teeth on the outer margin ( Fig. 4 C) and hind tibia yellowish on the basal two-thirds ( Fig. 4 E), in the male by the presence of hairs on the subcosta and much widened hind basitarsus as wide as or slightly wider than the hind tibia ( Fig. 5 D), in the pupa by the dorsal surface of abdominal segments 1–3 (rarely 1–4) darkened ( Fig. 6 C), and in the larva by the medium-sized postgenal cleft ( Fig. 7 C) and unicolored abdominal segments without dark transverse bands, though reddish-brown pigment present usually on the dorsal surface of segments 5 and 6. A combination of these characters separates this species from most other members of the S. asakoae species-group.

Females of S. (G.) asakoae were reported to bite humans (Choochote et al. 2005) and to serve as a vector of unknown filarial species in Thailand (Fukuda et al. 2003; Ishii et al. 2008).

Figures

FIGURE 4. Female of Simulium (Gomphostilbia) asakoae. A & B, Third segments of maxillary palps with sensory vesicles each having opening of different size (A, with opening of moderate size; B, with large opening; both right side and front view); C, Tip of mandible; D, Cibarium (front view); E, Hind tibia (left side; outer view); F, Hind basitarsus and second tarsomere (left side; outer view); G, Claw; H, Sternite 8 and ovipositor valve (right side only; ventral view); I, Genital fork (ventral view); J & K, Paraprocts and cerci (J, ventral view; K, lateral view); L, Spermatheca. Scale bars. 0.1 mm for E and F; 0.02 mm for A, B, D and H – L; 0.01 mm for C and G.

FIGURE 5. Male of Simulium (Gomphostilbia) asakoae. A & B, Third segments of maxillary palps with different shaped sensory vesicles (A, globular; B, ellipsoidal; A, right side; B, left side; both front view); C, Hind tibia (left side; outer view); D, Hind basitarsus and second tarsomere (left side; outer view); E, Coxites, styles and ventral plate (ventral view); F, style (right side; ventrolateral view); G, Ventral plate and median sclerite (lateral view); H, Ventral plate (caudal view); I, Median sclerite (caudal view); J, Paramere and aedeagal membrane (left side; caudal view); K & L, Abdominal segment 10 and cerci (right side; K, lateral view; L, caudal view). Scale bars. 0.1 mm for C and D; 0.02 mm for A, B and E – L.

FIGURE 6. Pupa of Simulium (Gomphostilbia) asakoae. A, Head and thorax (lateral view); B, Gill filaments (right side; outer view); C, Abdomen (dorsal view); D, Terminal hooks (caudal view); E, Abdomen (ventral view); F, Grapnel-shaped hooklet; G, Cocoon (dorsal view). Scale bars. 1.0 mm for G; 0.2 mm for A – C and E; 0.02 mm for D; 0.01 mm for F.

FIGURE 7. Larva of Simulium (Gomphostilbia) asakoae. A, B & C, Head capsules (A, dorsal view; B, lateral view; C, ventral view); D, Mandible; E, Hypostoma; F, Setae on dorsal surface of abdominal segment 8. Scale bars. 0.1 mm for A – C; 0.02 mm for D – F.