Limnorimarga limonioides ( Alexander, 1945 )

Podeniene, Virginija, Seo, Hong-Yul, Kim, Tae-Woo & Byun, Hye-Woo, 2017, First description of the last instar larva and pupa of the aquatic crane fly Limnorimarga limonioides (Alexander, 1945) (Diptera: Limoniidae), Zootaxa 4338 (2) : -

Limnorimarga limonioides ( Alexander, 1945)

( Figs. 1–26 )

Examined material: 2 reared males, 72 presumably last instar larvae, 1 male pupa, 2 male pupae exuviae, 3 female pupae from 5 localities near each other in Jirisan National Park: South Korea, Jeollanam-do province, Gurye , Toji-myeon , Naedong-ri , Piagol valley , N35.26580, E127.58128 / N35.25825, E127.58208 / N35.25257, E127.58981 / N35.26590, E127.58096 / N35.27448, E127.56378, altitudes 304–593 m, 24.iv–2.v.2015 ; 75 presumably last instar larvae, 1 male pupa, 2 male pupae exuviae, 6 female pupae, 9 female pupae exuviae from Gyeongju National Park: South Korea, Gyeongsangbuk-do province, Yangbuk-myeon, Janghang-ri , N35.76236, E129.36407, altitude 333 m, 28.v.2016 .

Description. Larva ( Figs. 1–11 ). Length 11.0– 13.8 mm; width 0.9–1.1 mm. Larvae hemicephalic, metapneunistic. Body covered with long dark brown hairs, giving body brown-greenish color ( Fig. 1 ).

Head capsule. Length 0.88–0.93 mm, width 0.57–0.63 mm, oval in shape, depressed dorsoventrally, slightly reduced, dorsal suture reaches one third of head capsule length ( Figs. 2, 3 ). Labrum trapezoidal with numerous sensory structures: small seta in the middle of anterior part, long seta next to it; sensory circle area with three sensory papillae inside below long seta ( Fig. 4 ). Clypeus distinctly divided from labrum, consisting of sclerotised narrow postclypeus, membranous square-shaped preclypeus. Frons separated from clypeus fused with internolateralia, wide, slightly sclerotised, except anterior part below antenna. Internolateralia heavily sclerotised. Two sensory pits and two long setae located between base of antenna and posterior part of preclypeus. Five sensory pits with short seta arranged in line situated in middle part of frons. Caudal end of frons rounded, without prominent spines ( Fig. 5 ). Basal segment of antenna cylindrical, more than three times as long as wide. Apical segment well developed, conical shaped ( Fig. 4 ). Sensory pit at one third of basal segment‘s length. Mandible triangular, with three large apical teeth similar in shape and size ( Fig. 6 ), three large teeth on ventral side and two small blunt teeth on dorsal side. Single long seta at base of mandible on outer edge, brush of hairs near base on inner edge. Maxilla well developed ( Fig. 7 ); inner maxillary lobe (lacinia + galea) and outer maxillary lobe (palpiger) large, similar in size. Outer maxillary lobe: apical part with short setae; button shaped apical papilla with sensory structures on apex, basal part sclerotised. Basal part of inner maxillary lobe bears two large and one small sclerite; sensory papilla on outer margin of uppermost sclerite; apical part covered with short setae and bears several prominent sensory structures on ventral side: elongated sensory structure with long seta apically on anterioapical part, large sensory papilla with small sensory structures inside in middle of anterior side, short sensory papilla below it and elongated sensory structure with long seta almost in middle of lobe. Cardo large, wedge shaped; large pore located in middle, long seta with large pore near outer margin of sclerite. Prementum dentated, labial area with single long and two short papillae in middle, large scale-like structures below them. Hypopharynx sclerotised, arch-shaped, toothless ( Fig. 8 ). Hypostoma bears 11 teeth. The middle tooth most prominent ( Fig. 9 ).

Thorax and abdomen. Abdominal segments II–VIII wider than longer. Thoracic and first abdominal segments short. Abdominal segments II–VII with dorsal and ventral creeping welts. Apical part of each welt bears numerous short, brown spinulae. Last abdominal segment (anal) constricted.

Anal division. Spiracular lobes reduced. Spiracular field rectangularly shaped fringed with short firm setae, not covered with setae or sclerites ( Fig. 10 ). Spiracle small and elongated. Distance between spiracles less than width of spiracle. Three long setae (length of each seta almost equal to the width of anal division) and one short setae on posterior end of anal division, four long setae on side (closer to posterior end) and one medium long seta on side near anterior end of anal division. Anus surrounded by twelve white, fleshy, finger-shaped equal sized anal papillae ( Fig.11 ). Length of each papilla almost equal to width of anal division. A long seta at base of anal papillae.

Pupa ( Figs. 12–26 ). Male pupae 8.5–9.2 mm long, 1.1–1.2 mm wide, female 9.0– 9.5 mm long, 1.1–1.2 mm wide. General forms of male and female pupae appear similar ( Figs. 12–17 ). Abdomen patchy colored, dorsum and sternum darker than pleuron. Abdomen of alive pupae pink hue. Head, thorax, wings, legs and terminal segment uniform in color, darker than the rest of body.

Head. Cephalic crest absent, surface smooth. Antennal sheaths short, not reaching base of wing ( Figs. 18–20 ). Clypeus flattened, inconspicuous, labrum oblong with bluntly rounded apex. Labial lobe oblong. Labial lobes adjacent to each other. Maxillary palp diamond-shaped, transversal ( Fig. 20 ).

Thorax. Pronotal horns large, close to each other, flattened, earlike and tapered anteriorly and posteriorly. Horn twice as long as wide. Dorsum of thorax smooth, sides of thorax forming fold above base of wing. Apex of wing reaching posterior margin of second abdominal segment ( Figs. 18, 20 ). Legs reaching posterior margin of third abdominal segment.

Abdomen. Segments III–VII divided by transverse fold into shorter anterior part and longer posterior part, anterior part of segments III–VII with dorsal and ventral creeping welts. Surface of abdominal segments smooth, tergum and sternum with 5–7 setae on posterior margin. Two setae on middle of pleuron. Spiracles hardly visible.

Terminal segment. Terminal segment of female elongate ( Figs. 21, 22, 23 ). Sheaths of cercus longer, wider than valve, flattened, with wavy ridge dorsally (as seen in lateral view in Fig. 21 ). No additional spines. Terminal segment of male blunt, narrow ( Figs. 24, 25, 26 ). Ventral lobes (anal spines) well developed, with rounded tips directed dorsally, reaching base of posterotergal spines. Posterotergal spines large, tapering into acute points directed upward. Sides of posterotergal spines flattened. Anterodorsal and mediodorsal spines absent, dorsal part of terminal segment with two knob-like tubercles.

Habitat ( Fig. 27 ). Larvae and pupae develop in gelatinous mass of algae accumulated on vertical wet stones irrigated with thin sheet of running water (fauna hygropetrica).

Discussion. The overall appearance of the larva of Limnorimarga is very similar to that of genera in the tribe Limoniini of the subfamily Limoniinae such as Geranomyia Haliday, 1833 , Limonia Meigen, 1803 , Dicranomyia Stephens, 1829 and Rhipidia Meigen, 1818 . The larvae of these genera all have the spiracular field with reduced lobes, and possess dorsal and ventral creeping welts. Genus Orimarga Osten Sacken, 1869 (tribe Antochini) also possess dorsal and ventral creeping welts, but it also has dorsal and ventral spiracular lobes. These genera do differ in the length and color of the hairs that cover the body surface. Larvae of all known species of Dicranomyia , Geranomyia , Limonia and Rhipidia are covered with short white hairs, while the body of Limnorimarga is covered with long dark brown hairs.

The number and shape of the anal papillae of Limnorimarga are unique among larvae of Limoniidae . Characteristically Limoniinae have two or four tubular or conus shaped anal papillae, the posterior pair shorter than the anterior pair. Limnorimarga has twelve equal-sized, finger-shaped anal papillae. Such a large number of anal papillae is unknown for the other genera of the family Limoniidae . In addition, differences among Dicranomyia , Geranomyia , Limonia , Rhipidia and Limnorimarga were noticed in the color and length of setae located on the posterior end of the anal division. Larvae of Dicranomyia , Geranomyia , Limonia and Rhipidia do not bear long and dark setae, while Limnorimarga has several long dark brown setae.

The general appearance of the head capsule of the larva of Limnorimarga is also very similar to that of genera of tribe Limoniini of subfamily Limoniinae such as Geranomyia , Limonia , Dicranomyia , Rhipidia and Metalimnobia Matsumura, 1911 . All these genera have oval and slightly reduced head capsules with short dorsal sutures. Differences were noticed in the shape of the terminal end of the frons. Larvae of almost all known species of Geranomyia , Limonia , Dicranomyia , Rhipidia and Metalimnobia have dentated terminal end of the frons, while in Limnorimarga the terminal end of the frons is rounded. Differences are noticed in the shape of the apical segment of the antenna. The apical segment of the antenna of Limnorimarga is well developed and cone-shaped, while the apical segment of Limonia , Dicranomyia , Rhipidia and Metalimnobia is short and button-shaped. Similar apical segment of antenna known also for Geranomyia canadensis (Westwood, 1836) ( Alexander & Malloch 1920). Limnorimarga bears 11 teeth on hypostoma, the same number of teeth as in Rhipidia , while Geranomyia , Limonia , Dicranomyia and Metalimnobia bear smaller number of teeth. The most significant differences in the head capsule are noticed in the hypopharynx. Limnorimarga has a sclerotised, archshaped hypopharynx, while the hypopharynx of all other Limoniini is dentate with teeth at apex.

As in the larva, the general appearance of the pupa of Limnorimarga is very similar to that of genera of the tribe Limoniini such as Geranomyia , Limonia , Dicranomyia , Rhipidia and Metalimnobia . Differences are seen in that Limnorimarga lacks a cephalic crest, the surface of the head and thorax is smooth, possesses dorsal and ventral creeping welts on abdominal segments III-VII, and the surface of the abdominal segments are smooth. Differences were noticed in abdominal coloration. Geranomyia , Limonia , Dicranomyia , Rhipidia and Metalimnobia have a uniformly colored abdomen, while in Limnorimarga the coloration is patchy.

Limnorimarga along with Geranomyia , Limonia , Dicranomyia , Rhipidia and Metalimnobia have flattened, very close to each other, ear-like pronotal horns, but size and shape varies slightly among them. The pronotal horns of Limnorimarga and Geranomyia canadensis are large with pointed ends, while in the other genera they are comparatively smaller with rounded ends. Limnorimarga has very short antenna (not reaching the base of wing), while in these other genera the antenna reaches the base of the wing or beyond that. The most significant difference was noticed in the shape of terminal segment in both sexes. The female pupa of Limnorimarga has flattened sheaths of the cerci with a wavy ridge dorsally, a unique feature for Limnorimarga within the subfamily Limoniinae . The male pupa of Limnorimarga has large posterotergal spines. Each spine is flattened laterally, with the tip sharply pointed and directed upward. This shape of the posterotergal spine is unique for Limnorimarga . In addition, Limnorimarga does not possess anterodorsal and mediodorsal spines, but the dorsal part of the terminal segment bears two knob-like tubercles as well as male pupa of Orimarga (Diotrepha) mirabilis .

Despite that Limnorimarga was described as part of Orimarga immatures of these two genera do not share many characters. Their larvae have different general appearance (except that they both have dorsal and ventral creeping welts) and different head capsules. Their pupae look different, except that male pupae of both genera lack anterodorsal and mediodorsal terminal spines.

Despite that several analyses have been made to solve the phylogenetical relationships of Tipuloidea ( Oosterbroek & Theowald 1991; Petersen et al. 2010) the genus Limnorimarga was not included in any of these analysis and relationships with other genera has remained unclear since the original description ( Alexander 1945). Characters of the larva and pupa of Limnorimarga allow preliminary placement of the genus in the cladogram of phylogenetic relationships of Tipuloidea based on larval and pupal characters through a nonquantitative analysis made by Oosterbroek & Theowald (1991). Limnorimarga belongs to tribe Limoniini as defined by synapomorphies 103 (larval segments 2 to 10 with creeping welts) and 104 (spiracular lobes reduced). It lacks synapomorphy 105 (caudal end of head capsule tridentate), but this character is also not present in several species of Limonia . This resemblance of immature stages of Limnorimarga to the immature stages of tribe Limoniini ( Dicranomyia group of genera) once again shows that classification based on characters of adults (were Limnorimarga belongs to tribe Antochini) and classification based on characters of preimaginal stages can give different results.

Larvae and pupae of Limnorimarga develop as typical fauna hygropetrica and they were found together with larvae and pupae of Geranomyia and Elliptera Schiner, 1863 .

Figures

FIGURE 27. Habitat of Limnorimarga limonoides (Piagol valley).

FIGURES 1 – 3. Limnorimarga limonioides, larva. 1: general view of larva, lateral aspect; 2: general view of head capsule, dorsal aspect; 3: general view of head capsule, ventral aspect.

FIGURES 4 – 9. Limnorimarga limonioides, larva. 4: labrum, clypeus, antennae and uppermost part of frons, dorsal view; 5: labrum, clypeus, antennae and frons, dorsal view; 6: right mandible, dorsal view; 7: right maxilla, ventral view, p—palpiger, i—inner maxillary lobe; 8: hypopharynx and prementum, ventral view, h - hypopharynx; 9: hypostoma, ventral view.

FIGURES 10 – 11. Limnorimarga limonioides, larva. 10: spiracular field; 11: anal field.

FIGURES 12 – 14. Limnorimarga limonioides, male pupa. 12: general view, dorsal aspect; 13: general view, ventral aspect; 14: general view, lateral aspect.

FIGURES 15 – 17. Limnorimarga limonioides, female pupa. 15: general view, dorsal aspect; 16: general view, ventral aspect; 17: general view, lateral aspect.

FIGURES 18 – 20. Limnorimarga limonioides, pupa. 18: head, thorax, I – III abdominal segments, lateral view; 19: head, thorax, I – II abdominal segments, dorsal view; 20: general view, lateral aspect, thorax, I – III abdominal segments, ventral view.

FIGURES 21 – 23. Limnorimarga limonioides, terminal segment of female pupa. 21: lateral view, c—cercus, v—valva; 22: dorsal view; 23: ventral view.

FIGURES 24 – 26. Limnorimarga limonioides, terminal segment of male pupa. 24: lateral view; 25: dorsal view; 26: ventral view, vl—ventral lobe, ps—posterotergal spine.