Phalacrocera replicata, (LINNAEUS, 1758)

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 : 1187-1189

PHALACROCERA REPLICATA (LINNAEUS, 1758)

( FIGS 5J , 10D , 18A, B )

Life history: Larvae were found to live in stagnant, dystrophic waters or acid pools of moors or woodlands where aquatic mosses, such as Hypnum , Fontinalis and Sphagnum , were abundant ( Bengtsson, 1897; Brindle, 1967; Brinkmann, 1997; Stubbs, 2010). Phalacrocera replicata had a single brood in a year ( Bengtsson, 1897; Müggenburg, 1901; Alexander, 1920); admittedly, they might have a second brood ( Miall & Shelford, 1897). Bengtsson (1897) confirmed that P. replicata moult at least eight and possibly ten times during their development. The first moult occurred 4–6 days after leaving the eggs ( Bengtsson, 1897), which did not significantly affect the external or internal appearance. The second moult occurred at about 18–20 days, and the larvae dramatically changed in appearance ( Bengtsson, 1897). First-instar larvae started feeding on the host-plants immediately after hatching; they scraped only the upper layer of leaves ( Peus, 1952). They overwintered as larvae and thus endured long and severe cold under the ice ( De Geer, 1773; Miall & Shelford, 1897; Wesenberg- Lund, 1915). The larvae were also able to live a long period of time (c. 5 days) in anoxic conditions ( Miall & Shelford, 1897) and they could sit down deep in water 1 m in depth for a while in autumn ( Wesenberg-Lund, 1915). Pupae were much more active than larvae and when disturbed, wriggled about and bent their bodies almost into a circle by flexion of the abdomen ( Miall & Shelford, 1897). Usually, the pupae rested vertically, with the mesothoracic horns reaching the surface of the water ( Miall & Shelford, 1897; Hemmingsen, 1952; Peus, 1952), by firmly grasping floating plants with its dorsal abdominal hooks ( Miall & Shelford, 1897). Although the pupae could survive asphyxiation for six hours ( Miall & Shelford, 1897), they occasionally floated at the water surface through weeds by abdominal movement, and then recovered their original position for respiration ( Miall & Shelford, 1897).

Oviposition behaviour: Larvae were found in ponds in which moss vegetation flourishes and currents keep the water in a constant motion ( Hemmingsen, 1952). Females walked on the water surface with the posterior end of the abdomen pricking into the water or into submerged moss ( Hemmingsen, 1952). Female adults deposited the eggs in the leaf axils of submerged moss, usually singly ( Miall & Shelford, 1897), or four to six egg batchs in each pocket of concave leaves of Fontinalis moss ( Wesenberg-Lund, 1943); the number of eggs laid in each leaf seemed to depend on the leaf size ( Hemmingsen, 1952). Females laid c. 60 eggs in total ( Miall & Shelford, 1897).

Egg: Spindle-shaped. Eggs of Phalacrocera appearently darkest among all genera ( Peus, 1952). Chorionic surface finely granulated, with numerous small pits ( Peus, 1952). Adhesive material delivered by the heads of club-shaped structures, and their necks stretched into apparent fibres when eggs are detached ( Hemmingsen, 1952).

Final-instar larva: Length 25 mm ( Brindle, 1967; Alexander, 1920). Body colour on dorsal side dark brown or lighter, showing dimorphism among individuals at final instar ( Wesenberg-Lund, 1915; Brinkmann, 1997; Pujante et al., 2016); dorsally with pale, indistinct stripes ( Miall & Shelford, 1897), and ventrally whitish. Body with extremely long cuticular lobes ( Fig. 16A ). Prothorax with each one pair of dorsal and lateral lobes; ventral lobe absent. Meso- and metathorax with dorsal and lateral lobes, filiform and long, two and one pair(s), respectively; one pair of ventral lobes, small and conical. Dorsal lobes on abdominal segments filiform and long, with length exceeding length of segment; segments I–VII with two pairs of lobes, anterior pair simple and posterior pair deeply bifurcated ( Fig. 5H ). Lateral lobes on abdominal segments simple without bifurcation, filiform and long; abdominal segment I with two pairs; abdominal segments II–VII with three pairs, anteriormost and posteriormost pairs shorter than middle pair, with longest pair approximate dorsal lobes in length. Ventral lobes on abdominal segments simple; segments I, II and III–VII with two, three, four pairs of lobes, respectively, posteriormost pair longest; additionally, on segments I–VII, single papilla-like lobe present near posterior end of segment. Anal segment with three pairs of lobes in total ( Fig. 16B ): one pair of dorsal lobes (dl), filiform and simple, bearing a short, sclerotized accessory lobe (dac) at the base with dark pigmentation; lateral lobe absent; one pair of ventral lobes (vl), blackened distally. Anal papillae soft and filiform, as single papilla (anp) on each side of the anus ( Fig. 8D ). Spiracular field without hair fringe ( Fig. 10D ). Elongated cuticular lobes internally containing tracheal branches ( Bengtsson, 1897; Peus, 1952).

Host-plants: This species feeds on submerged or aquatic mosses, including Sphagnum sp. ( Sphagnales : Sphagnaceae ) ( Clymo & Hayward, 1982), Amblystegium exanulatum De.Not. , A. fluitans Hedw. ( Hypnales : Amblystegiaceae ), Warnstorfia exannulata (Schimp.) Loeske ( Hypnales : Calliergonaceae ), Hypnum elodes F.Weber & D.Mohr (unsolved name) ( Hypnales : Hypnaceae ), Fontinalis antipyretica and F. dalecarlica Schimp. var. microphylla (Schimp.) Limpr. ( Hypnales : Fontinalaceae ) ( Miall & Shelford, 1897; Hemmingsen, 1952; Brinkmann, 1997). Miall & Shelford (1897) and Osten Sacken (1897) cited Engel (1884) and Giard (1895), who reported that the larvae not only eat some mosses (e.g. A. exanulatum ), but also aquatic angiosperms like Ranunculus fluitans Lam. ( Ranunculales : Ranunculaceae ), but this was not confirmed by later authors.

Larval behaviour: Larvae cling to moss stems using their large anal hooks to secure the body and sway it from side to side, as if to promote respiration ( Miall & Shelford, 1897). They creep from stem to stem by grasping with the mandibles and the anal hook alternately; when alarmed, they curl up like a caterpillar ( Miall & Shelford, 1897).

Figures

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 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 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 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.

Figure 18. Biology and structures of Phalacrocera replicata and P. tipulina. (A–B) P. replicata. (A) Specimen of lateinstar larva preserved in alcohol, dorsal view. (B) Characteristic lobes in anal segment, lateral view. (C–I) P. tipulina. (C) Specimen preserved in alcohol. (D) Late-instar larva curling its posterior body anchored with anal segment the Sphagnum mosses. (E) Late-instar larva floating near water surface with ventral side up, anchoring its mandibles to a moss shoot. (F) Morphological features of anal segment, oblique lateral view. (G) Ultrastructure of ventral lobe in anal segment, SEM view. (H) Ultrastructure of accessory dorsal lobe, SEM view.Abbreviations: anp, anal papilla; dac, accessory dorsal lobe; dl, dorsal lobe; dm, dorsomedial lobe; spd, spiracular disc; vl, ventral lobe. Scale (except G and H) = 1 mm.