Biodiversity Data Journal :
Single Taxon Treatment
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Corresponding author: Levente-Péter Kolcsár (kolcsar.peter@gmail.com)
Academic editor: Vladimir Blagoderov
Received: 26 Aug 2020 | Accepted: 23 Apr 2021 | Published: 01 May 2021
© 2021 Levente-Péter Kolcsár, Takeyuki Nakamura, Daichi Kato, Kozo Watanabe
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kolcsár L-P, Nakamura T, Kato D, Watanabe K (2021) Detailed description and illustration of larva, pupa and imago of Holorusia mikado (Westwood, 1876) (Diptera: Tipulidae) from Japan. Biodiversity Data Journal 9: e58009. https://doi.org/10.3897/BDJ.9.e58009
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Holorusia Loew, 1863 (Diptera: Tipulidae) is a relatively large crane fly genus with a wide distribution in the Afrotropic, Australasian–Oceanian, Eastern Palearctic, Oriental and Nearctic Regions. Although the genus is well known to include the largest crane fly species, the immature stages are, thus far, only described for the larva and pupa of the North American Holorusia hesperea Arnaud & Byers, 1990.
In this study, we describe for the first time the egg, larva and pupae of the Japanese Holorusia mikado (Westwood, 1876). Larvae were collected from semi-aquatic habitats, from slow flowing areas of streams and small waterfalls where leaf litter accumulates; the larvae are detritivores and feed on wet, decomposing leaves. The larvae were reared to adults in the laboratory. Morphological characters of immature stages discussed with comparison with the North American H. hespera. Male and female genitalia are illustrated and described in detail for the first time.
anal field, biology, chaetotaxy, ecology, head capsule, ovipositor, pupal sheath, spiracular field
Holorusia Loew, 1863 is a large genus of Tipulidae, with 115 species described thus far. The majority of Holorusia species are endemic to the Oriental Region (75 species), while the remaining species occur in the Australasian–Oceanian (20 species), Afrotropical (11 species), Eastern Palearctic (15 species) and Nearctic (one species) Regions (
The genus includes the largest known crane fly species, with one specimen of "Holorusia mikado", holding The Guinness World Record (2018) as “the world largest specimen of crane fly belonging to the species Holorusia mikado” (https://www.guinnessworldrecords.com/).
Exact systematic position of the genus Holorusia is not clarified so far. Early studies suggested a close relationship between Prionocera Loew and Holorusia; however, it was questioned by
The genus was revised by
The immature stages of the genus are currently only described for Western North American Holorusia hespera Arnaud et Byers, 1990 (=rubiginosa Loew, 1863) (
We collected the undescribed larvae of Holorusia mikado from the Honshu and Shikoku Islands and reared them in our laboratory. Here, we describe and illustrate the last instar larva, the pupae of both sexes, habitus and terminalia of the imagos and the unfertilised egg. The morphology of the larva and pupa was compared with those of the Nearctic H. hespera.
Larvae were collected by hand from a drainage ditch at the side of the road, stream banks, around small waterfalls and small springs in Japan (Fig.
Habitats of Holorusia mikado (Westwood, 1876). A. Small spring with loose, gravelly soil rich in detritus in Japan, Kochi Pref., Tosa, Higashiishihara, alt. 705 m, 33°41.74'N 133°26.51'E; B. Drainage ditch at the side of a mountain road with accumulated litter; C. Bank of stream with accumulated litter in Japan, Yamagata Pref., Oguni, Arakawa River Valley, alt. 340 m, 38°11.56'N; 139°48.2'E. Yellow arrows indicate exact locations where larvae were collected.
Male and female terminalia and larva head capsules were photographed in glycerol, after maceration with 10-15% potassium hydroxide (KOH) at room temperature. Pupal exuviae were cleaned in soapy water to remove dirt before photographing. A few larvae were killed by boiling water and preserved in 90% ethanol. Photos were taken using a Zeiss Stemi 508 stereomicroscope, equipped with a Canon Kiss M digital camera. Stack photos were combined using Zerene Stacker software. Illustrations were made in Adobe Photoshop CC 2019. Drawings were created by Takeyuki Nakamura.
The terminology used for larval and pupal morphological features follows
Depositories
CKLP Private collection of L.-P. Kolcsár
EMNS Echigo-Matsunoyama Museum of Natural Sciences, Tôkamachi, Japan
SCHU The Shirakami Research Center, Hirosaki University, Japan
Tipula mikado Westwood in
Holurusia mikado (Westwood) in
Ctenacroscelis mikado (Westwood) in
Holurusia mikado (Westwood) in
Descriptions of imago
Measurements. Body length: male 25–36 mm; female: 28–42 mm. Wing length: male 32–43 mm; female 32–42 mm.
Head. Yellowish-brown; ventral side of rostrum dark brown, with short brown setae (Fig.
Thorax. Yellowish-brown, with brownish and grey markings. Presutural area of scutum with three grey, longitudinal stripes; median stripe with a dark brown line in the middle; stripes surrounded with brown as in Fig.
Wing. Tinged with brown. Base of wing dark brown; Sc and R black proximal to crossvein h, remaining veins light brown to brown. Stigma inconspicuous. Calypter bare and well developed. Venation as in Fig.
Legs. Light brown to brown. Tips of femur and tibia each with a narrow black ring. Tip of femur with comb of dark, strong setae (Fig.
Leg parts of Holorusia mikado (Westwood, 1876). A. Tip of femur with comb of setae; B. Tip of the femur with comb of setae; C. Tip of tibia; D. Female fifth tarsomere, lateral view; E. Male fifth tarsomere, lateral view; F. Male fifth tarsomere, dorsal view; G. Male fifth tarsomere, ventral view. Scale bar: 0.5 mm (D–G).
Abdomen. Dark brown on both sexes (Figs
Male terminalia. Yellowish-brown to brown (Fig.
Male genitalia of Holorusia mikado (Westwood, 1876). A. Dorsal view; B. Ventral view; C. Lateral view; D. Sperm pump and aedeagus, lateral view; E. Sperm pump, anterior view. Abbreviations: ae – aedeagus, ag – aedeagal guide, aia – anterior immovable apodeme, ea – ejaculatory apodeme, pia – posterior immovable apodeme, gcx – gonocoxite, cg(ig) – clasper of gonostylus (inner gonostylus, lg(og) – lobe of gonostylus (outer gonostylus), tg9 – tergite 9, st – sternite 9. Scale bar: 1 mm (A–C).
Female terminalia. Light brown to brown Fig.
Female terminalia of Holorusia mikado (Westwood, 1876). A. Sternite 8 and hypogynial valves, dorsal view; B. ovipositor after sternite 8 and hypogynial valves removed, ventral view; C. Genital fork. Abbreviations: gc – genital chamber, ga(st9) – genital apodema/sternite 9, hv – hypogynial valve, spt – spermathecae, st – sternite. Scale bar: 1 mm.
Egg. A female laid, deformed, unfertilised eggs (not copulated with male) 5 days after it emerged from pupa. Shape of fertilised eggs may differ than that which is described below.
Eggs shiny black, 1.1–1.2 mm long, surface without granulation; micropylar opening (micropyle) at subapical protrusion or in small pit (Fig.
Description of last instar larva
Measurements. Length 45–55 mm (n = 11), width 6–7 mm (n = 11).
Head capsule. Length 4.5–5 mm (n = 4), width 2.5–2.8 mm (n = 4); oval in shape, massive tipulid type (Fig.
Lateral sclerotised plates of labrum close situated, distance less than 1/6 of plate width (Fig.
Anterior parts of head capsule of the last instar larva of Holorusia mikado (Westwood, 1876). A. labrum, frontoclypeus and antennae after maxillae and mandibles removed, dorsal view; B. anterior part of head capsule, dorsal view; C. anterior part of head capsule, ventral view. Scale bar: 0.5 mm.
Anterior part of clypeus weakly sclerotised. Eight setae around base of antenna; three equal in size, short setae, along outer side of frontal suture; five setae along inner side of frontal suture as: one long, pale seta near base of antenna, two small and one longer setae along frontal suture and one short seta near inner-laterally (Fig.
Mandible massive, rectangle in lateral view, with two sensory setae at base on lateral side (Fig.
Mouthparts of head capsule of last instar larva of Holorusia mikado (Westwood, 1876). A. Mandible, ventral view; B. outline of mandible, outer lateral view; C. Maxilla, ventral view. Not to scale. Abbreviations: bl – basal lobe of lacinia mobilis, c – cardo cmi – craniomandibularis internus, cme – craniomandibularis externus, lm – lacinia mobilis, pmx – maxillary palp. Scale bars: 0.5 mm (A and B); 0.5 mm (C).
Maxilla well developed; cardo triangular, slightly curved, with two pale, long setae near to distal end. Long seta with short base at membranous part of maxilla near the joinpoint of maxilla and hypostomal plate (Fig.
Prementum with five blunt teeth; labial area with two papillae on middle, ventral side covered by group of dense hairs originating from posterior premental margin. Hypopharynx membranous, more or less bilobed and covered by short, dense hairs. Hypophayngeal suspensoria (lateral arms of hypopharynx) sclerotised and curved apically (Fig.
Hypostomal plate with 9 teeth; middle tooth most prominent (Fig.
Thorax and abdomen. Living specimen greenish-brown, specimen stored in ethanol blackish-brown. Dorsum covered with micro and macro setae, not forming clear patches. Micro setae less dense on ventrum. Pleural area with dense setae, especially conspicuous in specimens stored in ethanol, due to shrinkage of the pleural area. Chaetotaxy of abdominal segment II–VII as in Fig.
Anal division and spiracular disc. Spiracular lobes subequal in length; ventral lobe slightly longer. Lobes capable of closing and hiding spiracles. Spiracles large, more than 1/3 as wide as spiracular disc. Margin of lobe fringed with long pale setae, base of setae black. Dorsal and ventral lobes with dark line along inner margin of lobe; lateral lobe with dark line along ventral margin. Lateral and ventral lobes with short black line, 1/3 of length of lobe. Dorsal lobe with a less noticeable line along the outer margin. Tip of ventral lobe with infuscated area. Sclerotised area ventrally to spiracle narrow line, length half of width of spiracle. Shade of patterns on lobes variable amongst specimens, delicated line on dorsal lobe sometimes difficult to recognise. (Fig.
Sensory setae are very short, very difficult to distinguish them. It is not clear if the short setae are bifid or two separate setae arising from each alveolus.
Dorsal lobe with alveolus at tip of lobe (Fig.
Anus surrounded by seven yellowish-brown, fleshy, long anal papillae. Three papillae on lateral side, one unpaired papilla at anterior margin of anus (Fig.
Description of pupa
Measurements. Length 35–50 mm (n = 4), width 5.5–6.5 mm (n = 4).
General colouration dirty brown. Pupal skin covered with fine particles of substrate (Fig.
Head. Antennal sheath short, as long as head sheath. Labrum sheath large, with transverse wrinkles; labial sheaths separated from each other; palpus sheath recurved (Fig.
Thorax. Respiratory horns 1.75 times longer than width of thorax in lateral view (Fig.
Abdomen. Pleurites flattened dorso-ventrally (Fig.
Male pupa. Last abdominal segment armed with six dorsal acute spine, equivalent to lobes of larval spiracular field (Fig.
Posterior end of pupa of Holorusia mikado (Westwood, 1876). A–C. male: A. dorsal view; B. lateral view; C. ventral view. D–F. female: D. dorsal view; E. lateral view; F. ventral view. Abbreviations: ad – anterio-dorsal spine, as – anal spine, cs – cerci sheath, gs – genital sheath, hvs - hypogynial valva sheath, ls – lateral spine, md – medio-dorsal spine, pd – posterio-dorsal spine, vls – ventro-lateral spine, vs – ventral spine. Scale bar: 2.5 mm.
Female pupa. Acute dorsal spines of last abdominal segment similar to those of male (Fig.
Japan: Honshu, Kyushu and Shikoku Islands.
Larval habitat and biology
Holorusia mikado larvae were collected from aquatic and semi-aquatic habitats. The larvae were found along the banks of mountain streams, waterfalls and in drainage ditches at the side of the road, where decaying litter accumulated and the water flow was relatively slow (Fig.
Larvae of aquatic Tipula (Nippotipula) are also known to occur and feed on decaying leaves (
Life cycle and activity
Four larvae of Holorusia mikado pupated almost in the same period, with about two and a half days between the earliest and latest pupations. Two males and two females emerged 7–8 days after the pupations, in the morning between 5 and 9 am. (Fig.
Flying period of imagos: Early May to late August.
Larva
The last instar larvae of H. mikado and H. hespera differ, particularly in the number of anal papillae and the pattern of the spiracular field. H. hespera has three-three lateral anal papillae, while H. mikado has an additional unpaired lobe between the lateral papillae, which is directed anteriorly (Fig.
Pupa
The pupae of H. hespera and H. mikado differ in the length of their respiratory horns, which are 1.75 times longer than the width of the thorax in H. mikado and about 1.25 times longer in H. hespera. The mid-leg sheath is slightly longer than the hind-leg sheath in H. hespera and clearly shorter than the hind-leg sheath in H. mikado (Fig.
The identification of “the largest specimen of crane-fly” as “Holorusia mikado”, registered by the Guinness World Records from China (Sichuan) is very questionable, based on the photos that are published on the internet. The specimen has a whitish scutellum and mediotergite, which is greyish-brown on H. mikado specimens. The Chinese specimen obviously belongs to another Holorusia species; therefore, we removed this species from the Chinese checklist. Although the Catalogue of the Craneflies of the World also lists H. mikado from the Island of Taiwan (
The authors would like to thanks collectors for valuable specimens. We would like to express our sincere thanks to Pjotr Oosterbroek (Leiden, Netherlands) for useful information about the distribution of Holorusia mikado and to JaeIck Jo (Fukushima, Japan) for the corrigenda the identification of Tipula (Nippotipula) species. We would like to thank Dr. Virginija Podeniene for reviewing the manuscript.
Kolcsár L.-P. was supported by the Japan Society for the Promotion of Science (JSPS) Postdoctoral Fellowships for Research in Japan (Short-term Program: PE18038 and Standard Program: P21094). This research was financially supported by the JSPS Grant-in-Aid for Scientific Research (Grant Numbers: 19K21996, 19H02276).