Indosialis bannaensis Liu, Yang & Hayashi, 2006

Piraonapicha, Kanyakorn, Sangpradub, Narumon, Jaitrong, Weeyawat & Liu, Xingyue, 2020, The alderfly genus Indosialis Lestage, 1927 (Megaloptera: Sialidae) in Thailand and Laos, with a description of a new species, Zootaxa 4786 (2), pp. 233-253 : 238-242

Indosialis bannaensis Liu, Yang & Hayashi, 2006

( Figs. 2–9 , 15 )

Indosialis bannaensis Liu, Yang & Hayashi, 2006: 33 , Figs. 1–7 ; Liu et al. 2008: 48 , Figs. 1 , 5–8 , 19; Bowles & Contreras-Ramos, 2016: 486 , Figs. 1–11 .

Type material. Holotype, male, China, Yunnan Province, Xishuangbanna National Reserve, Mengla, Shangyong , Longmen , 650 m a.s.l., 17.V.2005, X.Y. Liu ( CAU).

Other material examined. Thailand: 31 males, 61 females, 1 pupa, 5 larvae, Suriya Vithee Stream, Ta Phraya National Park, Lahan Sai District , Buriram Province, 14°13’43.79”N, 102°53’53.34’’E, 277 m a.s.l., 16. V.2017, K. Piraonapicha leg. ( KKU, THNHM) ; 3 larvae, Lam Ta Khlong Stream, Khao Yai National Park, Pak Chong District , Nakhon Raschasima Province, 14°25’26.24”N, 101°23’12.18’’E, 706 m a.s.l., 10.II.2019, K. Piraonapicha leg. ( KKU, THNHM) ; 1 male, Wang Tao Waterfall, Thap Lan National Park, Khon Buri District , Nakhon Raschasima Province, 14 o 20’13.64’’N, 102 o 14’48.00’’E, 223 m a.s.l., 24.IV.2014, K. Piraonapicha leg. ( KKU) ; 3 males, 3 females, 2 pupae, 3 larvae, Huai Lek Stream, Wang Saphung District , Loei Province, 17°21’9.76”N, 101°39’23.78’’E, 336 m a.s.l., 13. V.2019, K. Piraonapicha leg. ( KKU, THNHM) ; 1 male, 1 female, same locality and collector, 30. VI.2019 ( KKU) ; 1 male, 5 female, same locality and collector, 30.III.2020 ( KKU) ; 1 male, Khao Sok National Park , Surat Thani Province, 70 m a.s.l., secondary forest, bamboo forest, 6.XII.1991, P. Schwendinger leg. ( MNHG) ; 4 larvae, Sakaerat Expt. Sta. , 60 km S[outh]. Nakhon Ratchasima, Nakhon Ratchasima Province, 14°30’N, 101°55’E, 300–600 m a.s.l., 2–4. V.1971, P. & P. Spangler ( NMNH) ; 2 males, Chiangmai Province, 31.III.1953, M. Ratanopradith leg. ( NMNH) . Laos: 1 female, No. 49, [19]98, O. Merkl, G. Csorba leg. ( HNHM) ; 1 male, 5 km W[est]. Ban Toup, Bokeo Nature Reserve , Bokeo Province, 20°27–28’N, 100°45’E, 500–700 m a.s.l., 4–18. V.2011 ( NMB) ; 1 female, nr. Muang Khongxedon, Phou Xiang Thong NBCA, Saravan Province, 130 m, 25.II.2018, X.Y. Liu leg. ( CAU) .

Diagnosis. Head and prothorax orange in both sexes. Male. Inner margin of left mandible proximally with several small short setae; inner margin of right mandible with indistinct apical tooth followed by long and sharp preapical tooth and broad basal tooth; gonocoxite 9 in lateral view broadly rounded, with apex strongly narrowed and curved dorsad; ectoproct in lateral view subtriangular, with apex distinctly narrowed.

Description. Male (non-types, n = 10, Figs. 2–4 , 15 ). Body length 8.0 mm; right forewing length 7.5–8.0 mm; right forewing width 3.0 mm, right hind wing length 6.5–7.0 mm; right hind wing width 3.0 mm.

Head orange, subquadrate, slightly shorter than broad; dorsum of head with dense irregular raised scars on posterior half; labrum reddish brown, elliptical, shorter than broad, anterior margin distinctly concave, and covered with dense long erect setae; mandibles asymmetrical, smooth and shiny; left mandible with long and blunt apical tooth, followed by broad preapical tooth and several short setae on inner margin; outer margin of left mandible feebly convex ( Fig. 3A ); right mandible with indistinct (present as a denticle) apical tooth, followed by large, long and sharp preapical tooth and broad basal tooth on inner margin, with 4 short setae; outer margin of right mandible convex ( Fig. 3B ); clypeus orange, relatively short, and its anterior margin concave medially; compound eyes dark, relatively large and convex, located anterior to mid-length of head; scape and pedicel yellow, scape almost twice as long as pedicel, flagellum dark brown.

Thorax orange; pronotum (excluding anterior and posterior membranes) in dorsal view, subrectangular, slightly shorter than broad, with weakly convex lateral margins; setae on pronotum reddish brown; mesonotum in dorsal view, subrectangular, slightly shorter than metanotum. Wings grayish brown; veins brown, forewing about 2.5 times as long as broad; costal region with 5–7 distinct crossveins; hindwing slightly shorter than forewing, about 2.2 times as long as broad; costal region with 2 distinct costal crossveins; wings entirely covered with dense erect long setae mixed with dense very short setae. Legs covered with decumbent setae (setae on legs clearly longer than on wings); coxae brownish orange; femora, tibiae and tarsi brown (tarsi slightly darker than former two), pretarsal claws pale brown.

Abdomen reddish brown, abdominal segments 1–8 each with a pair of yellow spots medially.

Genitalia. Tergum 9 in dorsal view, subtrapezoidal, with anterior margin concave and posterior margin extensively concave; sternum 9 in ventral view, as long as broad, with anterior margin almost truncate and posterior margin extensively convex; gonocoxite 9 in lateral view, broad, ventral margin extensively convex, dorsal margin weakly convex on anterior half, and distal one third relatively narrowed and ditinctly curved dorsad; ectoproct in lateral view, subtriangular, distinctly narrowed distad and moderately curved inward; fused gonocoxites 11 in lateral view, with narrow gonostyli 11 directed posterodorsally; in dorsal view, gonostyli 11 present as a pair of slender spines, which are narrowed gradually to apex. Sac-like structure absent in male genitalia ( Fig. 4 ).

Female (non-types, n = 10, Figs. 2 , 3 , 5 ). Body length 9.0 mm; right forewing length 9.0– 9.5 mm; right forewing width 3.5–4.0 mm; right hindwing length 8–8.5 mm; right hindwing width 3.5–4 mm.

Similar to male in structure, sculpture, color, wing venation and pilosity, with the following condition that should be noted: Body slightly larger; mandibles symmetrical, each with large and blunt apical tooth, followed by medium-sized blunt tooth and very small triangular basal tooth on inner margin ( Fig. 3C ); sternum 7 broadly pentagonal in ventral view; gonocoxites 8 separated into a pair of subrectangular lobes, partly concealed under sternum 7; gonapophysis 8 subtrapezoidal, with some setae; gonocoxites 9 present a pair of broad ovoid valves, with small gonostyli 9 at tip; ectoprocts paired, small, and ovoid ( Fig. 5 ).

Pupa ( Figs. 6 , 7 ). Body length 9.0 mm. Exarate, curved inward in natural condition ( Figs. 6A, 6B ). Head in full-face view, orange, subquadrate almost as long as broad, with dense irregular raised scars on posterior half ( Fig. 7A ); labrum yellowish brown, subrectangular, anterior margin convex but incised medially ( Fig. 7B ); mandibles reddish brown, smooth and shiny, with large and sharp apical tooth, followed by medium-sized preapical tooth (digitiform) and a small subtriangular basal tooth (smaller than preapical tooth) on inner margin; outer margin of mandible roundly convex ( Fig. 7C ); antennae dark brown and filiform (white in early stage); compound eyes black, large, round, and convex. Pronotum orange, subrectangular, shorter than broad; mesonotum and metanotum broader than pronotum, both shorter than half of their width. Wing pad black. Coxae and trochanters orange; femora, tibiae and tarsi dark brown. Abdomen reddish brown, narrow, longer than head and thorax combined; each abdominal segment shorter than wide and clearly separated from each other by constrictions.

Pilosity: Dorsal portions of head and pronotum with sparse long orange erect setae mixed with short dark appressed setae; labrum with sparse long erect setae; antenna with dark appressed setae; each abdominal segment with dense sparse long erect setae.

Larva (last-instar, n = 3, Figs. 8 , 9 ). Body length excluding terminal filament 10.5 mm; terminal filament 4.0 mm. Campodeiform. Head yellowish to reddish brown, subquadrate; six stemmata small and flat; antenna pale yellow with four segments; first antennal segment (scape) about twice as long as wide; segment 2 longest, but slightly shorter than segments 3 and 4 combined; segment 3 slightly longer than segment 4; segment 4 with a slender and spine-like sensory peg ( Fig. 9A ); labrum yellowish brown, broad, anterior margin extensively convex bearing 18– 20 denticles ( Fig. 9B ); median portion of anterior labral margin with two pairs of short setae ( Fig. 9C ); mandibles yellowish brown, dentition same as in pupa, but tip of teeth sharper, and margins of preapical tooth serrate ( Fig. 9D ); in ventral view, cardo subtriangular, with a single seta at median portion; stipes with four setae, two along outer margin, one near inner margin, and one at median portion; lacinia curved inward, its inner margin with four setae (basal second seta longest); galea not segmented, with a seta near base; maxillary palpus with four segments, segment 1 shortest and shorter than broad, segment 2 longest, segment 3 slightly longer than segment 4; in ventral view, submentum with a pair of setae located at posterior one third approximately; mentum smaller than submentum, subpentagonal. Prementum subrectangular, slightly shorter than broad, with well-developed ligula; labial palpus with three segments, segment 1 as long as wide, with a seta apically ( Fig. 9E ). Thorax yellowish to reddish brown; pronotum rectangular, with dense small yellow spots; mesonotum and metanotum shorter than pronotum, twice as wide as long. Legs yellowish brown. Abdomen 10-segmented, reddish brown, with dense small yellow spots. Abdominal segment 1–7 each with a pair of lateral filaments; each lateral filament with 6 segments, covered with dense long setae. Terminal filament pale yellow covered with long setae.

DNA barcode data. In the maximum likelihood and neighbor-joining analyses showed the same results as shown in Fig. 16 . The male and female adults of I. bannaensis from Buriram, Loei and Nakhon Ratchasima Provinces were grouped together with the larvae and a single pupa examined here. Thus, these larvae and a pupa were confirmed to be I. bannaensis . The COI genetic distances in all samples of I. bannaensis ranged from 0 to 0.010 (GenBank Accession Numbers: MK578518 – MK578527 and MN087716 – MN087719 ).

Distribution. China (Yunnan), Laos (Bokeo, Saravan), Thailand (Chiang Mai, Phitsanulok, Loei, Kalasin, Nakhon Ratchasima, Buriram), Vietnam (Lam Dong) ( Fig. 17 ).

Biology. The biology of I. bannaensis adults is not known. Larvae are predacious and inhabit slow-flowing streams by burrowing into soft sediment or soil at the roots of aquatic plants especially Colocasia esculenta (L.) Schott ( Araceae ). Before pupating, the larvae leave the water and bury themselves in the soil along the bank. Pupation took 5–6 days at ambient temperature in the laboratory. The larvae of I. bannaensis seem to tolerate heavy metals. In Huai Lek stream, Loei Province, which previously carried the drainage from a gold mine, larvae of this species contributed approximately 49% of benthic macroinvertebrate density from a benthic macroinvertebrate sample in 2016 ( Sangpradub, 2017 identified as Sialis sp.), decreasing to 11% in 2019 after the gold mine ceased operation (NS unpublished data).

Remarks. Indosialis bannaensis is most similar to I. siamensis sp. nov. in the general appearance of male genitalia (see remarks under I. siamensis sp. nov.). This species is also similar to I. indicus Liu, Flint & Yang, 2008 in having an orange head and prothorax and the configuration of male ectoprocts. It can be distinguished from I. indicus by gonocoxite 9 of the male being distally narrowed and curved dorsad. This contrasts to I. indicus , where the male gonocoxite 9 is distally inflated but not distinctly narrowed and curved dorsad (see Liu et al. 2008).

Figures

FIGURE 1. Collection sites of Indosialis spp. in Thailand. A. Huai Lek Stream, Wang Saphung District, Loei Province; B. Lam Ta Khlong Stream, Khao Yai National Park, Pak Chong District, Nakhon Raschasima Province; C. Suriya Vithee Stream, Ta Phraya National Park, Lahan Sai District, Buriram Province; D. Wang Tao waterfall, Thap Lan National Park, Khon Buri District, Nakhon Ratchasima Province.

FIGURE 2. Indosialis bannaensis, lateral view. A. male; B. female. Scale bar: 5.00 mm.

FIGURE 3. Indosialis bannaensis, dorsal view. A. left mandible of male; B. right mandible of male; C. right mandible of female. Scale bar: 0.20 mm.

FIGURE 4. Indosialis bannaensis, male genitalia, A. dorsal view; B. ventral view; C. lateral view; D. caudal view. S9: sternum 9; gx9: gonocoxite 9; gst11: gonostylus 11; gx11: fused gonocoxites 11; T9: tergum 9; e: ectoproct. Scale bar: 0.50 mm.

FIGURE 5. Indosialis bannaensis, female abdominal apex, A. ventral view; B. gonapophysis 8, ventral view; C. lateral view. gx9: gonocoxite 9; S7: sternum 7; gx8: gonocoxite 8; gx9: gonocoxite 9; T7: tergum 7; T8: tergum 8; T9: tergum 9; e: ectoproct. Scale bar: 0.50 mm (A, C); 0.25 mm (B).

FIGURE 6. Indosialis bannaensis, pupa, A. early pupa, lateral view; B–D. late pupa B. lateral view; C. dorsal view; D. ventral view. Scale bar: 1.00 mm (C, D).

FIGURE 7. Indosialis bannaensis, pupa, A. head, anteroventral view; B. labrum, ventral view; C. right mandible, dorsal view. Scale bar: 0.50 mm (A); 0.25 mm (B, C).

FIGURE 8. Indosialis bannaensis, larva in dorsal view.

FIGURE 9. Indosialis bannaensis, larva, A. antenna; B. labrum, dorsal view; C. detail of apical portion of labrum, dorsal view; D. left mandible, dorsal view; E. maxillae and labium, ventral view. Scale bar: 0.25 mm (A, D, E); 0.20 mm (B); 0.05 mm (C).

FIGURE 15. Indosialis spp. Indosialis siamensis sp. nov. (A, C, E, G); Indosialis bannaensis (B, D, F, H). A, B. dorsal view; C, D. ventral view; E, F. lateral view; G, H. caudal view. Scale bar: 0.20 mm (A, C, E, G); 0.50 mm (B, D, F, H).

FIGURE 16. Molecular species delimitation of Sialidae using maximum likelihood (ML) and neighbor-joining (NJ) using partial COI sequences. Tree was inferred from 472 base pair of 19 species of Sialidae and a species of Corydalidae as the outgroup. Nodal support values are bootstrap values (percentage of 1000 replicate, left: ML; Right: NJ). Only nodes with bootstrap> 50% are indicated. Scale bar indicates 0.05 nucleotide substitutions. M: male adult; F: female adult; P: pupa; L: larva.

FIGURE 17. The map shows the geographical distribution of two Indochina Indosialis species. Indosialis bannaensis Liu, Yang & Hayashi, 2006 (●); Indosialis siamensis sp. nov. (■). The records from Phitsanulok, Kalasin Provinces (Thailand) are from Bowles & Contreras-Ramos 2016 and China and Vietnam (Liu et al. 2008).