Liogma brevipecten, ALEXANDER, 1932

Imada, Yume, 2021, Moss mimesis par excellence: integrating previous and new data on the life history and larval ecomorphology of long-bodied craneflies (Diptera: Cylindrotomidae: Cylindrotominae), Zoological Journal of the Linnean Society 193, pp. 1156-1204 : 1179

LIOGMA BREVIPECTEN ALEXANDER, 1932

( FIGS 1B, C , 2A, B , 4A , 5C , 6C , 7D–F , 8A–F , 9A–D , 10C , 11C, D , 15A–F )

Life history: This species is univoltine; adults emerge during May–July, in central Japan. Larvae of this species occur in well-moistened Mniaceae moss tufts in wet spots of forest or woodland, such as stream banks, trickling waters, rocks near waterfalls and lake margins. In Japan, they frequently co-occur with some other terrestrial moss-feeding species, such as L. serraticornis , L. mikado and T. kuwanai . In winter, the larva buries itself beneath the moss patches and sometimes its body is even embedded in the soft ground.

Egg: Length 0.9 mm (N = 1). Spindle-shaped, circular in cross-section, with a tapered front pole ( Fig. 2A ). Greyish yellow, apparently darker than T. kuwanai . Chorionic sculpture elongated and narrow, arranged as dotted dash lines; reticulated near micropyle (black arrowhead in Fig. 2A ).

First-instar larva: Length 2.8 mm (N = 3). Body hyaline ( Fig. 15E ). Dorsal elongated cuticular lobes on thoracic and abdominal segments simple, outer surface covered with simple microtubercles (mtb) ( Fig. 7C ). Dorsal lobes on thoracic and abdominal segments with spinules present but less apparent than in later-instar larvae.

Final-instar larva: Length 14 mm (N = 47). Body colour dark green dorsally, due to oblique dark pigmentation on lateral side ( Fig. 15A ); colour generally uniform among individuals, brown individual unknown. Integumental surface rugulose due to undulated or reticulated ridges ( Fig. 7D ). Prothorax with two pairs of dorsal lobes along pronotal ridge, small and conical, with needlelike apices; anterior opening relatively smooth, without distinct tubercles ( Fig. 15B ); one pair of lateral lobes near the posterior end of the segment, small. Meso- and metathoracic segments with one pair of dorsal lobes; lateral lobes two pairs; ventral lobes two pairs, small and conical. Dorsal lobes on abdominal segments with translucent, sharply pointed apices; lobe covered with numerous sharp, translucent spinules on anterior and posterior sides of the lobes ( Figs 6C , 7F , 15C ); abdominal segments I and II–VII with two and four pairs, respectively. Lateral lobes on abdominal segments with sharp apices; abdominal segment I with three pairs; abdominal segments II–VII with four pairs ( Fig. 5C ); lobes bearing spinules as of dorsal lobes, but with lower density. Ventral lobes on abdominal segments small and conical. Anal segment with one pair of dorsal lobes bearing spinules; one pair of ventral lobes, devoid of spinules; dorsomedial lobe absent; lateral lobe absent; two pairs of ventral lobes, anterior pair papilla-like; four anal papillae present. Spiracular field with hair fringe ( Fig. 10C ). Elongated cuticular lobes internally containing tracheal branches ( Fig. 15D ).

Oviposition: Behaviour of four female individuals was observed in the field (5–13 May 2016, at Kibune, Kyoto, Japan). The adults occur in humid moss patches in woodlands, where ground water exudes continually. At the locality, several acrocarpous mosses and Chrysosplenium grayanum Maxim. (Saxifragaceae) abundantly grow on the mucky soil. Females lay eggs singly, inserting the abdomen into the tufts of Rhizomnium and Mnium mosses. The eggs (N = 19) are laid exclusively on moss shoots.

Host-plants: Larvae are found from tufts of moss species belonging to Mniaceae (Bryales) . Recorded host-plants in the field include Plagiomnium acutum (Lindb.) T.J.Kop. , Pl. cuspidatum (Hedw.) T.J.Kop. , Pl. maximoviczii (Lindb.) T.J.Kop. , Pl. vesicatum (Besch.) T.J.Kop. , Rhizomnium hattorii T.J.Kop. and Rh. tuomikoskii T.J.Kop.

Figures

Figure 1. Life history of Cylindrotominae. (A) First-instar larva of Triogma kuwanai consuming fluid within a leaf of Plagiomnium vesicatum (Mniaceae), dorsal view; cells devoid of chlorophyll (black arrowheads) indicate the piercing-andsucking feeding method. (B) Final-instar larva of Liogma brevipecten chewing a leaf margin of Rhizomnium tuomikoskii (Mniaceae), lateral view; note that the head capsule is fully retracted within the lip-like cuticular lobe. (C) Pupa of Liogma brevipecten with a green hue and displaying transverse black stripes in abdominal segments, dorsal view. (D) Copulating couple of Liogma mikado on moss tufts; the female, on the left, was dragged out of the pupal exuvium by the male and thus the body has not been completely sclerotised. (E) Leaf of Stellaria (Caryophyllaceae) with two characteristic incisions in the epidermis of the lower leaf surface (white arrowheads) due to endophytic oviposition; the eggs are absent. (F) Egg of L. mikado laid on a shoot of Hylocomnium splendens (Hylocomniaceae). (G) Larva of C. japonica, which is being preyed upon by what is presumably a third-instar nymph of Himacerus apterus (Hemiptera: Nabidae). Scale = 1 mm.

Figure 2. Eggs of Cylindrotominae (Cylindrotomidae). (A) Liogma brevipecten, dorsal (left) and ventral sides (right); micropyle at the distal end (black arrowhead) and possess a lateral adhesive region (white arrowhead). (B) Liogma brevipecten on the lower side of a liverwort thallus of Conocephalum conicum (Conocephalaceae). (C) Triogma kuwanai, on a dicot shoot. Scale = 500 µm.

Figure 4. Coloration and patterning of larval Cylindrotominae. (A) Dissected integuments of larvae with a green hue of L. brevipecten (left) and L. mikado (right). Note that there is a marked difference in integument colouration between them and that L. mikado has a yellowish tint. (B) Final-instar larva of Cylindrotoma japonica drowned in a wet spot on a leaf. The transparency of the integument is evident, with a shiny, silvery ventral side. (C–D) Colour dimorphism in Liogma mikado. (C) Late-instar larva of Liogma mikado with a green hue, blending in well in a tuft of Plagiothecium euryphyllum (Plagiotheciaceae). (D) Late-instar individual with a brown hue, occurring on the same moss patch as (C).

Figure 5. Schematic diagram illustrating diverse arrangements and numbers of the elongated cuticular lobes in 11 cylindrotomine species. Each diagram represents a simplified larval body, longitudinally grouped into six, based on the patterned arrangements of the lobes: (1) prothorax, (2) meso- and metathorax, (3) abdominal segment I, (4) abdominal segment II, (5) abdominal segments III–VII, and (6) abdominal segment VIII (anal segment). Each square partitioned by double lines in a row denotes the integument on the dorsal (dl), lateral (la), ventral (vl) sides of the corresponding segment(s). Each black dot symbolizes a cuticular lobe, of which position/size in a given space express the relative position/size of the lobe.Anal papillae are not shown. Lobe forms, auxiliary outgrowths, and relative length of segments are not shown here (see each species' own description). Each taxon name is abbreviated. For G and I, diagrams are based on the description in Brodo (1967) and Peus (1952), respectively; caution is needed when these are compared with the species examined herein (A–F, I–K), because the lobe characteristics could be treated differently in the previous studies. For K, a single lobe is present at the location of asterisk (*) only in the abdominal segment VII but not in the other segments.

Figure 6. Comparative morphology of dorsal elongated cuticular appendages on abdominal segment in cylindrotomine larvae at late instar. (A) Cylindrotoma japonica. (B) Diogma glabrata. (C) Liogma brevipecten. (D) L. mikado. (E) L. nodicornis. (F) L. serraticornis. (G) Triogma kuwanai. (H) Phalacrocera replicata. For C, E and H, body colour is faded away due to preservation in alcohol. Scale = 1 mm.

Figure 7. Ultrastructure of dorsal integument, SEM views. Dorsal integument with elongated cuticular lobes of abdominal segment at larval stage. Cylindrotoma japonica (A–C). (A) General dorsal integument. (B) Dorsal elongated lobe. (C) Ditto, closer view. Liogma brevipecten (D–F). (D) General dorsal integument. (E) Dorsal elongated lobe, lateral side. (F) Ditto, frontal side. Phalacrocera tipulina (G–I). (G) General dorsal integument to which diatoms and debris are sparsely attached. (H) Ditto, closer view. (I) Dorsal elongated lobe. Scales are shown in each image.

Figure 8. Histological characterisation of internal structure of Liogma brevipecten at first instar, in crosssection. Different body segments are represented in each section: thoracic segments (A–C), showing foregut and midgut region; anterior (D) and posterior (E) parts of abdominal segments, representing anterior hindgut; and anal segment (F), illustrating posterior hindgut. Note that integumental thickness is heterogeneous across body parts. Black arrowheads and arrows denote intrinsic and extrinsic muscles, respectively. Abbreviations: cm, circular muscle; dcl, dorsal cuticular lobe; ddph, dorsal diaphragm; dv, dorsal blood vessel; ed, endocuticle; epd, epidermis; ept, gut epithelium; ex, exocuticle; fb, food bolus; ft, fat body; lcl, lateral cuticular lobe; lm, longitudinal muscle; lu, gut lumen; mdm, midgut microvilli; mlp, malpighian tubule; mtb, microtubercle; ne, ventral nerve cord; pr, peritrophic membrane; pro, proventriculus; re, rectum; sal, salivary duct; stm, stomodeal valve; tr, trachea; vdph, ventral diaphragm; vcl, ventral cuticular lobe. Scale = 50 µm.

Figure 9. Histological characterisation of internal structure of anal segment of Liogma brevipecten at first instar, in crosssection. Selected cross-sections of anal segment from anterior (A) to posterior (D), showing spiracular field and surroundings. Black arrowheads denote intrinsic muscles of lateral lobes.Abbreviations: anp, anal papilla; at, atrium chamber; re, rectum; stg, stigmal ring. Scale = 50 µm.

Figure 10. Spiracular lobes of cylindrotomine larvae. (A) Cylindrotoma japonica, dorsal view. (B) Liogma nodicornis, caudal view. (C) L. brevipecten, oblique dorso-caudal view. (D) Phalacrocera replicata, caudal view. (E) P. tipulina, caudal view. Abbreviations: anp, anal papilla; dac, accessory dorsal lobe; dl, dorsal lobe; dm, dorsomedial lobe; ha, hair fringe; sp, spiracle; spd, spiracular disc; vl, ventral lobe. Scale = 2 mm.

Figure 11. Ultrastructure of spiracular field of cylindrotomine larvae, SEM views. (A–B) Cylindrotoma japonica. (A) Spiracular field is devoid of hair fringe. (B) Ditto, closer view. (C–D) Liogma brevipecten. (C) Spiracular field is present on the lobe fringed with hairs. (D) Ditto, closer view. (E–F) Phalacrocera tipulina. (E) Spiracular field on the lobe with hair fringe. (F) Ditto, closer view. White arrowheads denote apertures in the central plugs. Scales are shown in each image.

Figure 15. Biology and morphology of Liogma brevipecten. (A) Final-instar larva, dorsolateral view. (B) Prothoracic integument sheltering the head capsule, frontal view. (C) Spinules on a dorsal lobe, dorsolateral view; for ultrastructure, see Fig. 6F. (D) Tracheal branches inserted into a lateral lobe. (E) First-instar larva, lateral view. (F) Female laying an egg onto the abaxial side of a leaf of Bryhnia novae-angliae (Brachytheciaceae). Scale = 1 mm.