Liogma mikado, (ALEXANDER, 1919)

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 : 1181

LIOGMA MIKADO (ALEXANDER, 1919)

( FIGS 1D, 1F , 3D , 4C, D , 5D , 6D , 16A–C )

Life history: Liogma mikado is univoltine, having the adult stage in spring. This species markedly differs in habitat preference from other Liogma species , although it frequently co-occurs with L. serraticornis on a small geographic scale (within a range of a few metres). The larvae are most frequently found on arid moss tufts on rocks or on the ground, but also on decomposed tree trunks. The larvae are exposed on the surface of moss patches, unlike other species of Liogma (e.g. L. brevipecten and L. serraticornis ), which sometimes bury deeply beneath the moss patches.

Mating and oviposition: Two adult females of L.mikado were observed during 13:00–16:10 on 19 May 2016, at Ikawa-touge (Shizuoka, Japan). The site was a forest floor with gentle slope facing a forest path toward a mountain pass. The males emerged before the females and waited beside the female pupae for the emergence of their mates. Mating took place mainly resting on the branches and leaves of the understory vegetation ( Fig. 1D ). When pairs are in copula, they readily take flight. The oviposition was observed once on the same day. One female flit about the tufts of mosses and lay an egg on a branch leaf of Hylocomnium splendens (Hedw.) Schimp. (Hylocomniaceae) ( Fig. 1F ).

Egg: Length 0.74 mm (N = 1). Nearly black in colour ( Fig. 1F ). Spindle-shaped, circular in cross-section, with a tapered front pole ( Fig. 2F ). Chorionic surface nearly black without noticeable wrinkles; sculptures unexamined.

First-instar larva: Length 1.3 mm (N = 2). Body hyaline ( Fig. 16B ). Dorsal elongated cuticular lobes on thoracic and abdominal segments simple and stout.

Final-instar larva: Length 8–10 mm (N = 3). Body colour polymorphic, with light green ( Fig. 4C ) or brown hue ( Fig. 4D ); dark pigmentation making a narrow band, appearing as an oblique line in lateral view, from mesothoracic through abdominal segment VII; also, tips of small lobes tinged, including lobes on thoracic segments, first and second pairs and auxiliary outgrowths (particularly, second and third teeth) of third and fourth pairs of lobes on abdominal segments II–VII ( Fig. 16A ). Integument slightly tinged yellow ( Fig. 4A ), surface smooth. Prothorax dorsally with two, conical pairs of lobes on pronotal ridge with sharply pointed apices, posterior pairs longer than anterior pairs; two pairs of lateral lobes, papilla-like. Meso- and metathoracic segments with two pairs of dorsal lobes, each with two conical auxilliary outgrowths at the front; two pairs of lateral lobes, anterior pair longer than posterior pair; one pair of ventral lobes, papillalike ( Fig. 5D ). Dorsal elongated lobes on abdominal segments generally short, longest lobe shorter than body width in ventrolateral view ( Fig. 6D ); segment I with two pairs: anterior pair conical, with two tiny teeth-shaped auxiliary outgrowths at the front; posterior pair long, with three teeth-shaped outgrowths at the front; segments II–VII with four pairs of lobes, anterior two pairs conical and simple, third pair with two teeth at the front and fourth pair with three teeth near the base at the front; apices of teeth-like auxiliary outgrowths obtuse and tuberculate when dried, sharply pointed when wet. Lateral lobes on abdominal segments with sharply pointed apices; segment I with three pairs, posterior two pairs longer than anteriormost pair; segments II–VII with four pairs, middle two pairs longer than others. Ventral lobes on abdominal segments small, rounded or conical. Anal segment with one pair of dorsal lobes, long; one pair of dorsomedial lobes, short and conical; lateral lobes papilla-like; two pairs of ventral lobes, anterior pair papilla-like. Spiracular field with hair fringe.

Host-plants: The host-plant range of this species varies considerably among populations. Typically, the larvae are found and reared on some species of Thuidium ( Hypnales : Thuidiaceae ), such as T. tamariscinum (Hedw.) Schimper , T. kanedae Sakurai , T. delicatulum (Hedw.) Schimp. , T. cymbifolium (Dozy & Molk.) Dozy & Molk. and T. pristocalyx (Müll. Hall.) Jaeger. In some populations, the larvae feed on Eurhynchium savatieri Schimp. ex Besch. ( Hypnales : Brachytheciaceae ), Hylocomiopsis ovicarpa (Besch.) Card. ( Hypnales : Leskeaceae ), Ctenidium capillifolium Brotherus , Hylocomnium splendens ( Hypnales : Hylocomniaceae), Hypnum oldhamii Jaeger ( Hypnales : Hypnaceae ), Thamnobryum sp. ( Hypnales : Neckeraceae ), Plagiothecium euryphyllum (Card. & Thér.) Iwats. and Pseudotaxiphyllum pohliaecarpum (Sull. & Lesq.) Iwats. ( Hypnales : Plagiotheciaceae ) ( Figs 4C, D , 16I ). Under rearing conditions, the following moss species are also detected from the faecal pellets of larvae: Leucobryum neilgherrense Müll. Hal. ( Dicranales : Dicranaceae ) and Fauriella tenuis (Mitt.) Cardot ( Hypnales : Theliaceae ). Thus, L. mikado potentially uses a wide range of mosses belonging to Hypnales , although no larva has ever been obtained from Bryales . From the faecal pellets, the larval diet exclusively consists of moss species, even though some liverworts, including Cephalozia ( Jungermanniales : Cephaloziaceae ) and Calypogeia ( Jungermanniales : Calypogeiaceae ), commonly occurred in the larval habitat.

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 3. Larvae of Cylindrotominae, showing diverse sizes and forms of elongated cuticular appendages. (A) Cylindrotoma distinctissima, ventral (left), lateral (middle), and dorsal (right) views. (B) Diogma glabrata, oblique ventral (left) and lateral (right) views. (C) Triogma trisulcata, oblique ventral (left) and dorsal (right) views. (D) L. mikado, lateral (left) and dorsal (right) view. (E) Phalacrocera tipulina, dorsal view. A–C are redrawn from Peus (1952).

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 16. Biology and morphology of Liogma mikado, L. nodicornis, L. serraticornis. (A–C) L. mikado. (A) Late-instar larva, lateral view. (B) First-instar larva (scale = 0.5 mm). (C) Early-instar larva on a tuft of Plagiothecium euryphyllum (Plagiotheciaceae). (D) Late-instar larva of L. nodicornis, feeding on Plagiomnium ciliare (Mniaceae). (E–I) L. serraticornis. (E) Late-instar larvae with green hue, feeding on Plagiomnium vesicatum (Mniaceae). (F) Late-instar larvae with brown hue feeding on Mnium lycopodioides (Mniaceae), found in the same population as the individual shown in (B). (G) Habitus of lateinstar, dorsal view; mesoand metathoracic segments are entirely dark and inverted Y-shaped pattern is evident in abdominal segments I–VII. (H) Characters of head. (I) Characters of anal segment. Black arrows indicate papilla-like, anterior pair of the ventral lobes. Abbreviations: anp, anal papilla; dl, dorsal lobe; pr, pronotal ridge; vl, ventral lobe. Scale (except B) = 1 mm.