Edaphologia, No. 102: 23–29, March 30, 2018 23

Redescripiton of japonicum Verhoeff, 1918 based on the type material (Crustacea, , )

Hiroki Yoshino, Kohei Kubota

Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan. Corresponding author: Hiroki

Yoshino ([email protected])

Received: 23 August 2017; Accepted 5 December 2017

Abstract Ligidium japonicum Verhoeff, 1918 is redescribed based on the type specimens in Verhoeff’s collection. The species is redefined on the basis of uropodal endopod that is 1.1 － 1.3 longer than exopod, pleopod 1 exopod with long setae, and pleopod 2 endopod with U-shaped apex, as well as presence of denticles on pleopod 2 endopod inner margin and one beak-shaped dent on outer margin at anterior position than cutout of inner margin. Variation in morphological characters is shown between type material and samples collected from Chiba prefecture.

Key words: Japan, morphological variation,

with the taxonomy of this species. Introduction Recently, we got a chance to examine the syntypes of The Ligidium Brandt, 1833 (Crustacea, Isopoda, L. japonicum deposited in the Zoologische Staatssammlung Ligiidae) contains around 50 species, most of which species München (ZSM), Germany, and herein we re-describe the live in very humid terrestrial habitats (Nunomura, 1983; morphological features of L. japonicum using this material. We Klossa-Kilia et al., 2006; Li, 2015, 2017). Six species inhabit also compare morphological characters between syntypes and Japan; L. japonicum Verhoeff, 1918, L. koreanum Flasarova, material collected in Chiba Prefecture, Japan, which belong to 1972, L. paulum Nunomura, 1976; L. ryukyuense Nunomura, the same species according to current diagnosis. 1983; L. kiyosumiense Nunomura, 1983; L. iyoense Nunomura, 1983 (Verhoeff, 1918; Nunomura, 1976, 1983). According to Nunomura (1983), L. japonicum is widely distributed in Materials and Methods Hokkaido, Honshu, Shikoku islands, and small satellite islands Ligidium japanicum syntypes: ca. 7 ♂♂22 ♀♀ and many in Japan, and its taxonomy is perplexed by the occurrence of particles in 70% ethanol, labeled as large variation in morphological features of the apical part of ‘LIGIDIUM japonicum Verhoeff, 1918/SYNTYPEN/ pleopod 2 endopod between Hokkaido and Honshu islands, a SYNTYPEN character that is considered important for species diagnosis of Hokkaido/Japan Ligidium species presently (Klossa-Kilia et al., 2006; Li, 2017). leg.: Sauter The original description of L. japonicum was given by Coll: VERHOEFF’. Verhoeff (1918) based on examination of 63 specimens from Hokkaido. Further, Jackson (1923) added some morphological With these syntypes, five slide preparations were made, characters based on specimens from‘ Moheri’ (?) in Japan. labeled‘ Ligidium japonicum Verh. 7. Per. Pleon. Japan. ♂’, However, these authors did not provide important information ‘Ligidium japonicum Verh. 2. 3. Per. u. L. (?) Pleontergiten on diagnostic features, such as the morphologies of the apex ♂’,‘ Ligidium japonicum Verh. Kopf, 1. 2. Per. Japan. ♂’, of pleopod 2 and mouth parts. In addition, Iwamoto (1943) ‘Ligidium japonicum Verh. Kopf, 1. Per. Japan, Sapporo ♂’, and Nunomura (1983) described the morphological features ‘Ligidium japonicum Verh. 7. Per. Pleop. Japan, Sapporo ♂’. of L. japonicum, but the descriptions did not refer to the type Because the conditions of the syntypes were bad and there specimens. Therefore the examination of the type specimens is no complete body of a male, we could not count exact of L. japonicum is very important for the resolving problems individual number, and avoided specifying the lectotype from 24 Hiroki Yoshino, Kohei Kubota

Fig. 1. Ligidium japonicum. Material from Mt. Nokogiriyama, male. Scale bars: 2 mm.

syntypes. towards 3 distal spines; second article about 1.4 times as Other material: Chiba Prefecture: 1 ♂ , Mt. Nokogiriyama, long as the first, with 3 trifid spines at distal tip; third article Futtsu City, Japan, Aug. 2, 2015, H. Yoshino leg.; 3 ♂♂, small, with 3 small setae (Fig. 2E). Antenna, peduncle with Kamisanagura, Tateyama City, Dec. 24, 2015, H. Yoshino 5 articles, first and second articles slightly shorter than third; leg.; 1 ♂ , Mt. Kanozan, Kimitsu City, Jul. 23, 2016, H. fourth article about twice as long as the third; fifth article Yoshino leg. about three times as long as the second; flagellum composed Morphological observations were conducted under a of 15 articles (Fig. 2F). stereoscopic microscope (CX41, OLYMPUS) using slides Left mandible with 3-toothed incisor; lacinia mobilis preparation and a scanning electron microscope (SEM: 3-toothed; 7 penicils between lacinia mobilis and molar JSM-6010, JEOL). All figures were drawn based on optical process (Fig. 2G). Right mandible with 3-toothed incisor; images. The pleopods 2 of the material we collected were lacinia mobilis of 14 denticles on distal margin; 4 penicils drawn starting with SEM photo. Morphological terminology between lacinia mobilis and molar process (Fig. 2H). followed Li (2015). Maxillule with inner lobe having 3 stout setulose setae of unequal size and one simple seta near distal margin; outer Redescription lobe with 10 (3 cleft) apical teeth and one stout plumose seta Ligidium japonicum Verhoeff, 1918 on distal margin (Fig. 2C). Maxilla with bilobed and setose [Japanese name: Nihon-hime-funamushi] apex, outer lobe much wider than inner lobe and bearing two (Figs. 1–5) stout subapical penicils (Fig. 2D). Maxilliped with rectangular endite bearing 7 penicils near distal margin and one tooth at Body elongated, 2.0–2.5 times as long as wide (Figs. 1, inner distal angle; palp with 5 articles; subrectangular epipod 2A); lateral margin of pereonites bears tiny setae, pereonites 1 with rounded apex (Fig. 2I). Most long setae of all pereopods and 2 without“ bristle field” on posterior margin of epimera. bifid (Fig. 3). Three short trifid setae on ventral side of Syntype material strongly decolorized. Coloration in the pereopod 1 carpus (Fig. 3H). Uropodal with protopod about material collected by us light brown to dark brown with or 2.5 times as long as broad; inner-distal projection of protopod without pale irregular spots, one dark longitudinal stripe as long as wide on its base; endopod 1.1–1.3 times as long as in middle of pereonites and pleonites, and one pale spot at exopod, with one long seta and one small seta; exopod with base of each pereonal epimera (Fig. 1). Cephalon yellow to two long setae (Fig. 4A). brown. Eyes black in color, each with approximately 80–90 Male. Pleopod 1 exopod triangular with one short seta ommatidia. Telson with rounded apex in the middle, concave and 3 to 5 long setae on distomedial margin, and 10 small near lateral margin, and forming blunted rounded corners (Fig. denticles on lateral part of distal margin (Fig. 4B); endopod 2B). with triangular distomedial projection bearing 4 to 5 long Antennule with first article subrectangular, broadened setae and no or one short seta (Fig. 4C). Pleopod 2 exopod Redescripiton of Ligidium japonicum 25

Fig. 2 Ligidium japonicum. syntype, male: A, Body in dorsal view (antenna and uropod lost); B, posterior margin of telson; C, maxillule; D, maxilla; E, antennule; F, antenna; G, right mandible in dorsal view; H, left mandible in dorsal view; I, maxilliped. Scale bars: A = 2 mm, B = 0.5 mm, C–E, G–I = 0.25 mm, F = 0.5 mm. 26 Hiroki Yoshino, Kohei Kubota

Fig. 3. Ligidium japonicum. syntype, male: A-G, pereopods 1-7; H, three short setae on carpus. Scale bars: A–G = 0.5 mm. Redescripiton of Ligidium japonicum 27

Fig. 4. Ligidium japonicum. syntype, male: A, uropod; B, pleopod 1 exopod; C, pleopod 1 endopod; D, pleopod 2; E, apical part of pleopod 2 endopod; G, pleopod 3 exopod; H, pleopod 3 endopod; I, pleopod 4 exopod; J, pleopod 4 endopod; K, pleopod 5 exopod; L, pleopod 5 endopod. Material from Mt. Kanozan, male: F, apical part of pleopod 2 endopod. Scale bars: A, D = 0.5 mm, B, C, E–L = 0.25 mm. 28 Hiroki Yoshino, Kohei Kubota

Fig. 5. Ligidium japonicum. Material from Mt. Kanozan, male: A, pleopod 2 endopod, ventral view, B, pleopod 2 endopod, dorsal view. Scale bars: A, B = 0.1 mm.

quadrangular with 2 setae on posterior margin (Fig. 4D); long as exopod, and pleopod 1 exopod with one short seta and endopod long, reaching or surpassing apex of pleopod 5, with three to five long setae. L. japonicum has telson with rounded folded, U-shaped apex of which outer margin with one beak- apex, pleopod 1 exopod with one short seta and 5 long setae, shaped dent at a more anterior position than cutout of inner and pleopod 1 endopod with 5 setae, while L. acutitelson has margin, and inner margin with obtuse-angled cutout and three telson with elongated and acute apex, pleopod 1 exopod with or four denticles in syntypes (Fig. 4E), or two, three, five, six, 5 long setae, and pleopod 1 endopod with 3 setae (Li, 2015). L. seven, or nine denticles in samples from Chiba Prefecture (Fig. japonicum can be distinguished from L, ryukyuense by pleopod 4F). 1 exopod with one short seta and 5 long setae, and apex of pleopod 2 endopod with denticles, whereas L. ryukyuense Type locality has pleopod 1 exopod with 3 setae, and apex of pleopod 2 Hokkaido, Japan (Verhoeff, 1918). Since‘ Sapporo’ endopod with no denticle (Nunomura, 1983). L. japonicum was written in the labels of two out of five prepared slides, is most similar to L. koreanum in telson with rounded apex, ‘Sapporo City, Hokkaido Prefecture, Japan’ seems to be the the shape of antennule, right mandible with 3-toothed incisor exact type locality of L. japonicum. and lacinia mobilis, 4 penicils between lacinia mobilis and molar process, pleopod 1 exopod triangular with long setae on Remarks distomedial margin and small denticles on lateral part of distal Ligidium japonicum Verhoeff, 1918 was similar to L. margin, inner-distal projection of uropodal protopod as long acutangulum Li, 2015, L. acutitelson Wang & Kwon, 1993, as width of its base, uropodal endopod and exopod ending L. burmanicum Verhoeff, 1946, L. deltodontum Li, 2017, L. with two setae, and apex of pleopod 2 endopod with denticles denticulatum Shen, 1949, L. formosanum Wang & Kwon, 1993, at inner margin (Flasarova, 1972). However, L. japonicum L. gracilentum Li, 2017, L. inerme Nunomura & Xie, 2000, L. has eye with about 80–90 ommatidia, left mandible with jiushai Tang & Zhou, 1999, L. koreanum Flasarova, 1972, L. 7 penicils between lacinia mobilis and molar process, and polyacanthum Li, 2017, L. ryukyuense Nunomura, 1983, and pleopod 2 endopod of which U-shaped apex with two to nine L. sichuanense Nunomura, 2002 in having pereonites 1 and 2 denticles on inner margin and one beak-shaped dent on outer without bristle field on posterior margin of epimera (Verhoeff, margin at anterior position than cutout of inner margin, while L. 1946; Borutzky, 1950; Wang and Kwon, 1993; Tang and Zhou, koreanum has eye with 110 ommatidia, lacinia mobilis of left 1999; Nunomura and Xie, 2000; Nunomura, 2002; Li, 2015, mandible with 6 penicils between lacinia mobilis and molar 2017). However, L. japonicum can be distinguished from L. process, and pleopod 2 endopod with narrowed apex, one to acutangulum, L. burmanicum, L. deltodontum, L. denticulatum, two denticles on inner margin and one beak-shaped dent on L. formosanum, L. gracilentum, L. inerme, L. polyacanthum, outer margin at beginning of cutout of inner margin. and L. sichuanense by uropodal endopod 1.1 － 1.3 times as We found that L. japonicum collected from Chiba Prefecture Redescripiton of Ligidium japonicum 29 showed variation in denticle number (2–9) on the apex of Sfenthourakis S. and Parmakelis, A., 2006. Molecular pleopod 2 endopod, while syntype material have three or four phylogeny of the Greek populations of the genus Ligidium denticles. A more complete sample collection across the whole (Isopoda, Oniscidea) using three mtDNA gene segments. distribution is necessary to understand the morphological Zoologica Scripta, 35(5): 459–472. variation of this species. Li, W. C., 2015. Ligidium acutangulum sp. nov., a new species of terrestrial Isopoda (Oniscidea, Ligiidae) from China. Acknowledgements Crustaceana, 88(1): 18–26. Syntype material of Ligidium japonicum described in Li, W. C., 2017. Morphology and molecules reveal high species this paper was kindly provided by Dr. Stefan Fridrich of the diversity of Ligidium (Crustacea: Oniscidea: Ligiidae) in ZSM. We thank Dr. Harufumi Nishida (Chuo University) Jiangxi, China. Zoological Journal of the Linnean Society, and Dr. Julien Legrand (Chuo University) for the rental of a 179(3): 627–641. microscope and technical support. Nunomura, N., 1976. Ligidium paulum, a new terrestrial isopod from Ashu, Kyoto Prefecture, Japan. Bulletin of Osaka 摘 要 Museum of Natural History, 30: 1–4. 吉野広軌・ 久保田耕平（東京大学農学生命科学研究科 Nunomura, N., 1983. Studies on the terrestrial isopod 〒 113-8657 東京都文京区弥生 1-1-1）：タイプ標本に基づいた in Japan. I. Taxonomy of the families Ligiidae, Trichoniscidae ニホンヒメフナムシの再記載． and Olibrinidae. Bulletin Toyama Science Museum, 5: 23–68. タイプ標本に基づいてニホンヒメフナムシLigidium Nunomura, N., 2002. Two new species of the genus Ligidium japonicum を再記載した．ニホンヒメフナムシは以下の点で再 (Isopoda: Ligiidae) from Sichun Province, Southwest China. 定義される：尾肢内肢が尾肢外肢の 1.1–1.3 倍である，第 1 腹 Special Bulletin of the Japanese Society of Coleopterology, 5: 肢外肢に長い刺毛がある，第 2 腹肢内肢の先端は U 字である， 41–49. 内側に複数の棘がある，内側の切り欠きの前方の外側には棘 Nunomura, N. and Xie, R., 2000. Terrestrial isopod crustaceans of が一つある．第 2 腹肢内肢の先端の内側の棘の数の変異がタ Yunnan, Southwest China. pp. 43–89, In: Taxonomical studies イプ標本と千葉県の標本の間で見られた． on the soil fauna of Yunnan Province in Southwest China. (eds. キーワード：日本，形態変異，分類 Aoki, J., Yin, W. and Imadaté, G.), Tokai University Press, Tokyo. References Tang, B. P. and Zhou, K. Y., 1999. A new species of the genus Borutzky, E. V., 1950. Soviet Biospeleology XII. Terrestrial Ligidium (Isopoda, Oniscidea) from China. Crustaceana, Isopoda in the caves of the Caucasus and the Crimea. I. Fam. 72(1): 17–24. Ligiidae. 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