Simulium darjeelingense

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 : 53-60

4) Simulium darjeelingense species-group

Simulium (Gomphostilbia) eshimai Takaoka & Adler sp. nov.

Female. Body length 2.0 mm. Head. Slightly narrower than thorax. Frons brownish black, densely covered with yellow scale-like recumbent short hairs and few dark hairs along each lateral margin; frontal ratio 1.8:1.0:1.8; frons:head ratio 1.0:3.7. Fronto-ocular area well developed, narrow, directed dorsolaterally. Clypeus brownish black, slightly white pruinose, and densely covered with yellowish-white recumbent hairs interspersed with several dark longer hairs on each side. Labrum 0.8 times as long as clypeus. Antenna composed of scape, pedicel and nine flagellomeres, dark brown, though scape, pedicel and base of first flagellomere slightly lighter. Maxillary palp composed of five segments, light brown except third segment dark brown, proportional lengths of third, fourth, and fifth segments 1.0:1.1:2.2; third segment ( Fig. 22 A) somewhat enlarged; sensory vesicle ( Fig. 22 A) elongate, 0.5 times length of third segment and with medium-sized opening. Maxillary lacinia with 13 or 14 inner and 20 outer teeth. Mandible with 36 inner teeth and four or five outer teeth at some distance from apex. Cibarium ( Fig. 22 B) with dorsal margin having short plate produced forward and downward, and with weakly-sclerotized mediolongitudinal stripe bearing well-sclerotized U-shaped ridge apically. Thorax. Scutum brownish black, slightly shiny when illuminated at certain angles, densely covered with yellow scale-like recumbent hairs mixed with whitish similar hairs on peripheral portions. Scutellum dark brown, covered with yellow short hairs and darkbrown long upright hairs. Postnotum brownish black, white pruinose and slightly shiny when illuminated at certain angles, and bare. Pleural membrane bare. Katepisternum longer than deep, dark brown, white pruinose and shiny when illuminated at certain angles, moderately covered with pale and dark short hairs. Legs. Foreleg: coxa yellow; trochanter light brown except base yellow; femur medium brown with apical cap dark brown (though extreme tip yellow); tibia medium brown except base yellow and apical cap dark brown, though median portion of outer surface widely lighter; tarsus brownish black to black, with moderate dorsal hair crest; basitarsus somewhat dilated, 7.0 times as long as its greatest width. Midleg: coxa medium brown except posterolateral surface dark brown; trochanter light brown except base yellow; femur medium brown except basal one-fourth yellow and apical cap medium brown (though extreme tip yellow); tibia medium to dark brown except extreme base yellow and apical cap brownish black; tarsus dark brown to brownish black, though base of basitarsus somewhat lighter. Hind leg: coxa medium brown; trochanter yellow; femur light to medium brown except base yellow and apical cap dark brown (though extreme tip yellow); tibia light to medium brown except base yellow, apical cap dark brown and subbasal portion medium to dark brown; tarsus ( Fig. 22 C) dark brown except basal two-thirds of basitarsus (though base light brown) and little less than basal half of second tarsomere whitish; basitarsus ( Fig. 22 C) narrow, slightly narrowed toward apex, 7.6 times as long as wide, and 0.64 and 0.54 times as wide as greatest widths of tibia and femur, respectively; calcipala ( Fig. 22 C) well developed, slightly longer than wide, and 0.6 times as wide as greatest width of basitarsus; pedisulcus ( Fig. 22 C) well developed; claw ( Fig. 22 D) with large basal tooth 0.5 times length of claw. Wing. Length 1.5 mm. Costa with dark-brown spinules and light-brown hairs except basal patch of yellow hairs. Subcosta haired except near apex bare. Hair tuft on base of radius dark brown intermixed with several yellow hairs. Basal portion of radius fully haired. Basal cell absent. Halter . Creamy except basal stem darkened. Abdomen. Basal scale grayish yellow, with fringe of yellowish-white hairs. Dorsal surface of abdomen medium brown except segment 2 grayish yellow though tergal plate medium brown, and 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 creamy, those of other segments ochreous except sternite 8 dark brown; sternal plate on segment 7 undeveloped. Terminalia . Sternite 8 ( Fig. 22 E) bare medially, with 12–14 medium-long to long hairs together with few slender short hairs on each side. Ovipositor valve ( Fig. 22 E) triangular (though posteromedial corner appearing to be truncated), thin, membranous, moderately covered with microsetae interspersed with three or four short hairs; inner margins nearly straight or sinuous, with small depression subapically, moderately sclerotized, and somewhat separated from each other. Genital fork ( Fig. 22 F) of usual inverted-Y form, with slender stem; arms of moderate width, with lateral plate angulated anterodorsally. Paraproct in ventral view ( Fig. 22 G) with anteromedian margin slightly raised ventrally, with unpigmented anteromedial surface having four or five sensilla; paraproct in lateral view ( Fig. 22 H) much produced ventrally, 0.6 times as long as wide, with 18 or 19 medium-long to long hairs on ventral and lateral surfaces. Cercus in lateral view ( Fig. 22 H) short, rounded posteriorly, 0.5 times as long as wide. Spermatheca ( Fig. 22 I) ellipsoidal, 1.6 times as long as greatest width, well sclerotized except duct and small area near juncture with duct unsclerotized, and with many fissures on surface; internal setae absent; both accessory ducts slender, subequal in diameter to major one.

Male. Body length 2.2–2.5 mm. Head. As wide as thorax. Upper eye medium brown, with large facets in 16 or 17 vertical columns and 17 horizontal rows. Face brownish black, whitish-gray pruinose when illuminated at certain angles. Clypeus brownish black, whitish-gray pruinose when illuminated at certain angles, and moderately covered with yellow short hairs interspersed with 12–16 dark-brown longer hairs on each side. Antenna composed of scape, pedicel and nine flagellomeres, brownish black except base of first flagellomere light brown; first flagellomere elongate, twice length of second one. Maxillary palp with five segments, light brown except third segment dark brown, proportional lengths of third, fourth, and fifth segments 1.0:1.1:2.1; third segment ( Fig. 23 A) somewhat widened apically; sensory vesicle ( Fig. 23 A) ellipsoidal, medium-long, 0.3 times length of third segment, and with opening of medium-size. Thorax. Scutum black, slightly shiny when illuminated at certain angles, densely covered with golden-yellow short hairs. Scutellum brownish back, with golden-yellow short hairs and dark-brown long upright hairs. Postnotum brownish black and bare. Pleural membrane bare. Katepisternum longer than deep, brownish black, thinly pruinose and slightly shiny when illuminated at certain angles, moderately covered with dark hairs. Legs. Foreleg: coxa and trochanter medium brown; femur medium brown with apical cap dark brown; tibia medium brown except apical cap dark brown and medial portion of outer surface light brown: tarsus brownish black; basitarsus slightly flattened, 9.1 times as long as greatest width. Midleg: coxa dark brown except posterolateral surface brownish black; trochanter medium brown; femur medium brown with apical cap dark brown (though extreme tip somewhat paler); tibia medium brown except base dark yellow and apical cap dark brown, and with golden-yellow short hairs on posterior surface of basal one-third; tarsus dark brown to brownish black. Hind leg: coxa dark brown; trochanter light brown; femur medium brown with apical cap dark brown (though extreme tip yellow); tibia medium brown to brownish black except base dark yellow to light brown; tarsus dark brown except basitarsus grayish to light brown and little less than basal half of second tarsomere whitish; basitarsus ( Fig. 23 B) enlarged, spindle-shaped, 4.2 times as long as wide, and 0.9 and 1.0 times as wide as greatest widths of tibia and femur, respectively; calcipala ( Fig. 23 B) well developed, slightly longer than width at base, and 0.4 times as wide as greatest width of basitarsus; pedisulcus ( Fig. 23 B) well developed. Wing. Length 2.2 mm. Other characters as in female except costa without basal patch of yellow hairs, subcosta bare, and hair tuft on base of radius dark brown. Halter . Ochreous with basal portion darkened. Abdomen. Basal scale brownish black, with fringe of dark-brown long hairs. Dorsal surface of abdomen dark brown to brownish black, covered with lightbrown short to long hairs; segments 2, 6 and 7 each with pair of shiny dorsolateral patches, when illuminated at certain angles; ventral surface of segment 2 grayish white, those of other segments medium to dark brown. Genitalia. Coxite in ventral view ( Fig. 23 C) nearly rectangular, 1.7 times as long as its greatest width. Style in ventral view ( Fig. 23 C) slender, curved inward, tapered toward middle, with apical spine; style in ventrolateral view ( Fig. 23 D) 0.9 times as long as coxite, tapered from base to middle, then nearly parallel-sided toward apex, with round apex. Ventral plate in ventral view ( Fig. 23 C) transverse, 0.7 times as long as greatest width at base, with body narrowed posteriorly, with anterior margin produced anteromedially, posterior margin concave medially, and densely covered with microsetae on ventral surface except anterolateral areas bare; basal arms of moderate length, somewhat divergent, then convergent apically; ventral plate in lateral view ( Fig. 23 E) with posterior portion of body not produced ventrally; ventral plate in caudal view ( Fig. 23 F) slightly rounded ventrally (width:height=1.0:0.3), with dorsal margin concave medially, densely covered with microsetae on posterior surface. Median sclerite ( Fig. 23 C, E, G) plate-like, arising from level near anteromedial tip of ventral plate, and directed dorsally. Paramere ( Fig. 23 H) with four distinct hooks. Aedeagal membrane ( Fig. 23 H) moderately covered with microsetae, and with no sclerotized dorsal plate. Ventral surface of abdominal segment 10 ( Fig. 23 I, J) without distinct hair near posterior margin on each side. Cercus ( Fig. 23 I, J) rounded, slightly produced ventrally, with 17 or 18 hairs.

Pupa. Body length 2.3–2.5 mm. Head. Integument yellow, moderately covered with small round tubercles except most of ventral surface of face bare; antennal sheath without tubercles; frons with three pairs of unbranched long trichomes with straight apices; face with two pairs of unbranched long trichomes with straight apices ( Fig. 24 A); three frontal trichomes on each side arising close together, subequal in length to one another and nearly as long as or somewhat longer than facial ones. Thorax ( Fig. 24 B). Integument yellow, moderately covered with round tubercles on anterior one-third, and almost bare on other portion except dorsal surface near posterior margin sparsely covered with small tubercles; thorax with three long anterodorsal trichomes with coiled or straight apices, two anterolateral trichomes with straight apices (anterior one medium-long, posterior one long), one long mediolateral trichome with straight apex, and three ventrolateral trichomes with straight apices (anterior one medium-long, two others long) on each side; all trichomes unbranched. Gill ( Fig. 24 B, C) composed of eight slender thread-like filaments, arranged in three groups (one dorsal, one ventral inner and one ventral outer) arising from short common basal stalk, which has somewhat swollen basal fenestra; dorsal group composed of three filaments all arising upward at same level from short stalk, ventral inner group composed of one individual and two paired filaments with short primary and secondary stalks, or all three filaments arising forward at same level from short stalk, and ventral outer group composed of two paired filaments with short stalk; all filaments light brown, subequal in length (0.7–1.0 mm) and thickness to one another except ventral filament of ventral pair somewhat thicker than others when compared basally; cuticle of all filaments without annular ridges and furrows, and densely covered with minute tubercles. Abdomen. Dorsally, all segments nearly unpigmented and without tubercles except segments 1 and 2 pale yellowish, and segment 9 and basal portions of spine-combs on segments 6–9 yellowish; segment 1 with one unbranched slender medium-long hair-like seta on each side; segment 2 with one unbranched slender medium-long or short hair-like seta and five short somewhat spinous setae submedially near posterior margin on each side; segments 3 and 4 each with four hooked spines and one short somewhat spinous seta near posterior margin on each side; segments 5–8 each with two or three unbranched short setae near posterior margin on each side; segments 6–9 each with spine-combs in transverse row and comb-like groups of minute spines near anterior margin; segment 9 with pair of cone-like terminal hooks ( Fig. 24 D). Ventrally, segment 4 with one unbranched hook and few unbranched short setae on each side; segment 5 with pair of bifid or trifid hooks submedially and few unbranched short slender setae on each side; segments 6 and 7 each with pair of bifid or trifid inner and unbranched outer hooks somewhat spaced from each other and few unbranched short slender setae on each side; segments 4–8 with comb-like groups of minute spines. Each side of segment 9 with three grapnel-shaped hooklets. Cocoon ( Fig. 24 E). Wall-pocket-shaped, moderately woven, widely extended ventrolaterally; anterior margin thickly woven, without anterodorsal bulge or projection; posterior half with floor roughly or moderately woven; individual threads visible; 3.0 mm long by 2.6–2.8 mm wide.

Mature larva. Body length 4.0– 4.6 mm. Body light ochreous except anterior surface of thoracic proleg, thoracic segment 3 (except ventral surface light ochreous) and abdominal segments 1–4 entirely greenish, and ventral surface of abdominal segments 5–9 creamy (though light-ochreous transverse band on ventral surface of segment 7). Head. Head capsule whitish yellow, with no distinct head spots, and sparsely covered with unpigmented minute setae (though moderately on dorsal surface); ventral surface slightly darkened near lateral margins of postgenal cleft, and with negative elongate spot on each side of postgenal cleft. Antenna composed of three articles and apical sensillum, longer than stem of labral fan; proportional lengths of first, second, and third articles 1.0:0.8:0.7–0.8. Labral fan with 42 primary rays. Mandible ( Fig. 25 A) 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 acute angle against mandible on apical side; supernumerary serrations absent. Hypostoma ( Fig. 25 B) with row of nine apical teeth, of which median tooth is longer than each corner tooth; lateral margin smooth; four or five hypostomal bristles per side lying nearly parallel to or slightly divergent posteriorly from lateral margin. Postgenal cleft ( Fig. 25 C) arrow-head-shaped, long, 4.2 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 moderately covered with dark setae with two to five branches (majority of setae with three or four branches) interspersed with unbranched colorless setae (similar to those in Fig. 25 D) on dorsal surface, abdominal cuticle of segments 1–4 sparsely covered with similar branched dark minute setae on dorsal surface, and that of segments 5–9 densely covered with dark minute setae each with two to eight branches (majority of setae with four to six branches) interspersed with unbranched colorless setae ( Fig. 25 D) on dorsal and dorsolateral surfaces, even on dorsal surface of each side of anal sclerite; last abdominal segment densely covered with unbranched colorless longer setae on dorsolateral and lateral surfaces of each side of anal sclerite and on each lateral surface down to base of ventral papilla; thorax and abdomen without dorsal protuberances. Rectal scales present, unpigmented. Rectal organ compound, each of three lobes with several finger-like secondary lobules (exact number of secondary lobules uncountable). Anal sclerite of usual X-form, with anterior arms 1.1 times length of 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 85–88 rows of hooklets with up to 13 or 14 hooklets per row.

Type material. HOLOTYPE: Female (with its associated pupal exuviae and cocoon) in 80% ethanol, labeled in a vial as [ UMSRP: Vietnam 0 30, Holotype, Simulium (G.) eshimai , Female, coll. Vietnam, 20-XII-2014, Takaoka et al.], reared from a pupa collected from a river (width 6 m, depth 0.6 m, bottom rocky, water temperature 11.0˚C, exposed to the sun, elevation 1,728 m, 22˚22’22.719”N/103˚45’24.852”E) fast-flowing in forest, Lai Chau, Sapa , Lao Cai Province, northern Vietnam, 20-XII-2014, by H. Takaoka, M. Sofian-Azirun, Z. Ya’cob, C.D. Chen & K.W. Lau . PARATYPES: Two males, three pupal exuviae, one mature larva, same data as those of the holotype in 80% ethanol, labeled in a vial as [ UMSRP: Vietnam 0 30, Paratype, Simulium (G.) eshimai , coll. Vietnam, 20- XII-2014, Takaoka et al.]; one mature larva in 80% ethanol, labeled in a vial as [ UMSRP: Vietnam 0 30, Paratype, Simulium (G.) eshimai , coll. Vietnam, 20-XII-2014, Takaoka et al.], collected from a small cascading stream (width 2.5 m, depth 3 cm, bottom rocky, water temperature 11.0˚C, exposed to the sun, elevation 1,853 m, 22˚21’18.609”N/103˚46’27.550”E) slow-flowing in forest, Oguy Ho, Sapa , Lao Cai Province, northern Vietnam, 20-XII-2014, by H. Takaoka, M. Sofian-Azirun, Z. Ya’cob, C.D. Chen & K.W. Lau.

Biological notes. The pupae of this new species were collected from plastic sheets in the current. Associated species were S. (M.) nigrofilum sp. nov., S. (N.) laichauense sp. nov., S. (N.) tayense sp. nov., S. (S.) rosliramlii sp. nov. and S. (S.) turgidum sp. nov.

Distribution. Vietnam (Lao Cai).

Etymology. The species name eshimai is in honor of Prof. Nobuoki Eshima, Kyoto University, for his great contribution to statistical analysis of infectious diseases and long-standing support of our studies of black flies.

Remarks. This new species is placed in the S. darjeelingense species-group (five species included) of the subgenus Gomphostilbia , defined by Takaoka (2012), based on the fore coxae darkened, male hind basitarsus enlarged ( Fig. 23 B), ventral plate not produced ventrally ( Fig. 23 E, F) (its ratio of the height against the greatest width is 0.33), and pupal gill with eight short slender filaments ( Fig. 24 B).

This new species shows great similarities to S. (G.) chayamaritae Takaoka & Srisuka from Thailand ( Takaoka and Srisuka 2010) in many characters including the number of male upper-eye facets, male genitalia ( Fig. 23 C), arrangement of pupal gill filaments ( Fig. 24 B) and pupal face with an additional trichome on each mediolateral surface ( Fig. 24 A). However, this new species is distinguished from the latter species by the round tubercles on the frons (frons with cone-shaped tubercles each with a sharply-pointed apex in S. (G.) chayamaritae ). There is no information on the additional trichomes on the pupal face of the four other species of the S. darjeelingense speciesgroup.

This new species is distinguished from S. (G.) darjeelingense Datta from India ( Datta 1973), S. (G.) guizhouense Chen, Zhang & Yang from China ( Chen et al. 2003a), and S. (G.) guniki Takaoka from Sabah, Malaysia ( Takaoka 2001b) by the pupal gill filaments arranged as 3+3+2 or 3+(1+2)+2 ( Fig. 24 B) (2+(2+2)+ 2 in S. (G.) darjeelingense and S. (G.) guizhouense , and all eight filaments arising at the same level from the common basal stalk in S. (G.) guniki ). Simulium (G.) darjeelingense also differs from this new species by the number of male upper-eye facets (in 14 vertical columns and 14 horizontal rows), and absence of pupal terminal hooks.

The remaining species, S. (G.) xizangense An, Zhang & Deng from China, which was described from a male ( An et al. 1990), differs from this new species by the small round sensory vesicle and ventral plate slightly widened posteriorly.

Figures

FIGURE 22. Female of Simulium (Gomphostilbia) eshimai sp. nov. A, Third segment of maxillary palp with sensory vesicle (right side; front view); B, Cibarium (front view); C, Hind basitarsus and second tarsomere (left side; outer view). D, Claw; E, Sternite 8 and ovipositor valve (left side only; ventral view); F, Genital fork (ventral view); G & H, Paraprocts and cerci (G, ventral view; H, lateral view). I, Spermatheca. Scale bars. 0.1 mm for C; 0.02 mm for A, B and D – I.

FIGURE 23. Male of Simulium (Gomphostilbia) eshimai sp. nov. A, Third segment of maxillary palp with sensory vesicle (right side; front view); B, Hind basitarsus and second tarsomere (left side; outer view); C, Coxites, styles and ventral plate (ventral view); D, Style (right side; ventrolateral view); E, Ventral plate and median sclerite (lateral view); F, Ventral plate (caudal view); G, Median sclerite (caudal view); H, Paramere and aedeagal membrane (left side; caudal view); I & J, Abdominal segment 10 and cerci (right side; I, lateral view; J, caudal view). Scale bars. 0.1 mm for B; 0.02 mm for A and C – J.

FIGURE 24. Pupa of Simulium (Gomphostilbia) eshimai sp. nov. A, Head (left side; outer view); B, Thorax and gill filaments (left side; outer view); C, Basal portions of gill filaments (left side; dorsal view); D, Terminal hooks (caudal view); E, Cocoon (dorsal view). Scale bars. 1.0 mm for E; 0.1 mm for A and B; 0.05 mm for C; 0.02 mm for D.

FIGURE 25. Larva of Simulium (Gomphostilbia) eshimai sp. nov. A, Mandible; B, Hypostoma; C, Head capsule (ventral view); D, Setae on dorsal surface of abdominal segment 8. Scale bars. 0.1 mm for C; 0.02 mm for A, B and D.