Japanese Journal of Systematic Entomology, 22 (2): 203–207. November 30, 2016.

Three Oriental Species of the Genus Enicospilus Stephens (: : Ophioninae) Newly Recorded from Japan

So SHIMIZU 1), 2) and Kaoru MAETO 1) 1) Laboratory of Biodiversity and Ecosystem Science, Graduate School of Agricultural Science, Kobe University, Rokkodaicho 1–1, Nada, Kobe, Hyogo 657–8501, Japan. 2) Corresponding author: [email protected]

Abstract Three species of the ophionine genus Enicospilus Stephens, 1835 collected in the Ryukyu Islands, E. abdominalis (Szépligeti, 1906), E. nigronotatus Cameron, 1903, and E. xanthocephalus Cameron, 1905, were newly recorded from Japan. E. abdominalis and E. xanthocephalus are widely distributed in the Oriental region and its neighbouring areas, however E. nigronota- tus is endemic to the Oriental region. Most of the specimens were collected in light traps, and thus the species are presumed to be nocturnal.

Introduction (SMZ1500, Nikon, Tokyo, Japan) was used for morphological observation. Multi-focus photographs for figure 1 were taken The genus Enicospilus Stephens, belonging to the tribe using a single-lens reflex camera (D90, Nikon, Tokyo, Japan) Enicospilini Townes of the ichneumonid subfamily Ophioninae and were stacked by using Zeren Stacker. Figure 2 was taken Shuckard (Townes, 1971; Rousse et al., 2016), comprises over using a digital microscope (VHX-600, Keyence, Osaka, 700 species that are distributed in all biogeographical regions Japan). All figures were edited by Adobe Photoshop© CS5. except for the Arctic (e.g., Yu et al., 2012; Broad & Shaw, 2016). The morphological terminology mainly follows Gauld It is the solitary koinobiont endoparasitoid of middle- to large- (1991) and Gauld & Mitchell (1981). The abbreviations and sized lepidopterous larvae (e.g., the families Lasiocampidae, indices used in this study follow Shimizu et al. (2016) as Noctuidae, and Saturniidae) (e.g., Gauld & Mitchell, 1981; listed below. Yu et al., 2012) and is prospering in tropical regions (Gauld & Mitchell, 1981; Gauld, 1985). Adult wasps have the “ophionoid Abbreviations facies”, characterised by the long antennae, large ocelli, orange- F – female (FF – females) brown body, and so on (Gauld & Huddleston, 1976), and are M – male frequently collected in light traps, like other nocturnal wasps T – metasomal tergite (e.g., Gauld & Mitchell, 1981; Short et al., 2006). LT– light traps A total of 36 species of the genus have been previously recorded in Japan (Yu et al., 2012; Watanabe & Yamauchi, Indices 2014). However, there are many unrecorded or undescribed AI (Alar index of fore wing) = length of 1m-cu between 2m- species, and we have recently recognised three unrecorded cu and bulla / length of 3rs-m species found in the collections from the Ryukyu Islands. CI (Cubital index of fore wing) = length of Cu1 between 1m- Hence, we record them for the first time from Japan herein. cu and Cu1a / length of Cu1b ICI (Intercubital index of fore wing) = length of 3rs-m / length Materials and methods of M between 2m-cu and 3rs-m SDI (Second discoidal index of fore wing) = length of Cu1a The abbreviations for depositories are listed below. between Cu1b and 2m-cu / length of Cu1 between Rs+M ANIC – Australian National Insect Collection, Canberra, and 1m-cu Australia BMNH – Natural History Museum, London, England EUM – Ehime University Museum, Matsuyama, Japan KPMNH – Kanagawa Prefectural Museum of Natural History, Subfamily Ophioninae Shuckard, 1840 Odawara, Japan Tribe Enicospilini Townes, 1971 MUC – Marathwada University Collection, Aurangabad, India Genus Enicospilus Stephens, 1835 NIAES – National Institute for Agro-Environmental Sciences, Tsukuba, Japan Enicospilus Stephens, 1835: 126. Type-species: OMNH – Osaka Museum of Natural History, Osaka, Japan merdarius Gravenhorst sensu Stephens (= Ichneumon SEHU – Laboratory of Systematic Entomology of Hokkaido ramidulus Linneaus), by subsequent monotypy (Stephens, University, Sapporo, Japan 1845). See Gauld & Mitchell (1978, 1981) and Gauld TARI – Taiwan Agricultural Research Institute Council of (1977, 1985, 1988) for detail synonym lists. Agriculture, Executive Yuan, Taichung, Taiwan TM – Termeszettudomanyi Muzeum, Budapest, Hungary Generic diagnosis. This genus is characterised by the The specimens examined are deposited in EUM, KPMNH, following combination of character states: mandible weakly NIAES, OMNH, and SEHU. A stereoscopic microscope

Ⓒ Japanese Society of Systematic Entomology 204 Shimizu, S. and K. Maeto

Fig. 1. Lateral habitus of Enicospilus species, new to Japan. (a) E. abdominalis (Szépligeti), female; (b) E. nigronotatus Cameron, male; (c) E. xanthocephalus Cameron, female. All from Okinawa Pref. to strongly tapered and twisted; ocelli large, usually adjacent (Figs. 1a, 2a) with eyes; occipital carina present; posterior transverse carina of mesosternum complete; discosubmarginal cell of fore wing Henicospilus abdominalis Szépligeti, 1906: 138. Holotype: F, with glabrous area and sometimes with sclerites (Figs. 1, 2); Sri Lanka (TM). ramellus of fore wing usually absent (Figs. 1, 2); fore tibial Ophion semiopacus Matsumura, 1912: 114. Holotype: F, spur without a membranous flange; outer distal margin of mid Taiwan (SEHU) [examined]. Synonymized by Gauld & and hind trochantelli usually without a tooth; and ovipositor Mitchell (1981). usually short (Fig. 1). Distribution. Afrotropical, Australasian, Nearctic, Diagnosis. This species is easily distinguished from any Neotropical, Oceanic, Oriental, and Palaearctic regions (Yu et other Japanese species of the genus because of its striking al., 2012). body colour (Fig. 1a). This also has the following combination Bionomics. The following lepidopterous families are known of character states that distinguishes it from any other species: as hosts: Apatelodidae, Arctiidae, Brachodidae, Drepanidae, yellow-brown interocellar area; outer surface of mandible Geometridae, Lasiocampidae, Lymantriidae, Noctuidae, without a diagonal groove; notauli absent; sclerites and Notodontidae, Papilionidae, Pyralidae, Saturniidae, Sesiidae, fenestra of discosubmarginal cell as in Fig. 2a; proximal part Sphingidae, and Tortricidae (Yu et al., 2012). The following of marginal cell of fore wing entirely hirsute (Fig. 2a); cu-a of tenthredinoid families are also known as hosts: Diprionidae fore wing proximal to base of Rs+M (Fig. 2a); Rs+2r of fore and Tenthredinidae (Yu et al., 2012). Adult wasps are often wing weakly sinuous (Fig. 2a); AI = 0.5–0.8 (Fig. 2a); CI = collected in light traps (e.g., Gauld & Mitchell, 1981). 0.1–0.3 (Fig. 2a); ICI = 0.6–0.8 (Fig. 2a); SDI = 1.3–1.4 (Fig. Remarks. We have examined many Japanese specimens 2a); Cu1 of hind wing complete; mid and hind trochantelli of the genus deposited in the EUM, KPMNH, NIAES, SEHU, simple without a decurved tooth; hind tarsal claw simply TARI, and so on. As a result, many unrecorded or undescribed pectinate and distal pecten without longer than true apex of species were recognised from Japan. claw; anterior part of T1–4 yellow-brown and posterior part dark brown to black (Fig. 1a). Enicospilus abdominalis (Szépligeti, 1906) Distribution. Australasian (Papua New Guinea), Oriental [New Japanese name: Torafu-hoshi-amebachi] (China, India, Japan*, Malaysia, Philippines, Sri Lanka,

November 30, 2016, JJSE 22 (2) New records of three Enicospilus species 205

Borneo (BMNH), designated by Townes et al. (1961). Henicospilus triguttatus Uchida, 1928: 221. Holotype: F, Taiwan (SEHU) [examined]. Synonymized by Gauld & Mitchell (1981).

Diagnosis. This species is distinguished from any other species of the genus by the following combination of character states: orange interocellar area; notauli absent; sclerites and fenestra of discosubmarginal cell as in Fig. 2b; proximal part of marginal cell of fore wing entirely hirsute (Fig. 2b); cu-a of fore wing subopposite to base of Rs+M (Fig. 2b); Rs+2r of fore wing weakly sinuous (Fig. 2b); AI = 1.1–1.6 (Fig. 2b); CI = 0.7–1.0 (Fig. 2b); ICI = 0.7–1.5 (Fig. 2b); SDI = 1.2–1.3 (Fig. 2b); Cu1 of hind wing complete; mid and hind trochantelli simple without a decurved tooth; hind tarsal claw simply pectinate, and distal pecten without longer than true apex of claw. Distribution. Oriental (Brunei, China, Japan*, Malaysia, Philippines, Singapore, Sri Lanka, and Taiwan) region (Yu et al., 2012). *New record. Bionomics. Unknown. Remarks. This is one of the largest species (i.e., fore wing ca. 20 mm in length) of the genus. Specimens examined. JAPAN: 1F, Genka-Arume-rindô, Nago City, Okinawa Is., Okinawa Pref., 31. VII. 2013, H. Ogai leg. (EUM); 1M, same data except for 4. IX. 2013 (EUM) (Figs. 1b, 2b).

Enicospilus xanthocephalus Cameron, 1905 [New Japanese name: Minami-hoshi-amebachi] (Figs. 1c, 2c)

Enicospilus xanthocephalus Cameron, 1905: 122. Holotype: F, Sri Lanka (BMNH). Enicospilus bullatus Chiu, 1954: 53. Holotype: F, Taiwan (TARI) [examined] Synonymized by Gauld & Mitchell (1981). Enicospilus obliquus Chiu, 1954: 54. Holotype: M, Taiwan (TARI) [examined] Synonymized by Gauld & Mitchell Fig. 2. A part of the fore wing of Enicospilus species, new to (1981). Japan. (a) E. abdominalis (Szépligeti), female; (b) E. nigronotatus Enicospilus paraclinatus Nikam, 1975: 198. Holotype: M, Cameron, male; (c) E. xanthocephalus Cameron, female. All from India (MUC). Synonymized by Nikam (1980). Okinawa Pref. Enicospilus pexus Gauld, 1977: 86. Holotype: F, Australia (ANIC). Synonymized by Gauld & Mitchell (1981). Taiwan, and Thailand), and Eastern Palaearctic (Korea) regions (Yu et al., 2012). *New record. Diagnosis. This species resembles E. flavocephalus (Kirby, Bionomics. Virtually unknown, while, the specimen 1900) in Japan but is distinguished from it and any other examined in this study was collected in a light trap. species of the genus by the following combination of character Remarks. A single specimen collected in Okinawa Island states: black interocellar area; notauli absent; sclerites and of the Ryukyu Islands was recognised. fenestra of discosubmarginal cell as in Fig. 2c; proximal part Specimen examined. JAPAN: 1F, Nûha, Ôgimi Vil., of marginal cell of fore wing entirely hirsute (Fig. 2c); cu-a of Kunigami County, Okinawa Is., Okinawa Pref. [26° 41' 21.3" fore wing opposite to base of Rs+M (Fig. 2c); Rs+2r of fore N, 128° 09' 01.3" E; ca. 200 m alt.], 29–30. VI. 2016, S. wing weakly sinuous (Fig. 2c); AI more than 1.50 (Fig. 2c); CI Shimizu et al. leg. (LT) (NIAES) (Figs. 1a, 2a). = 0.3–0.5 (Fig. 2c); ICI = 0.3 (Fig. 2c); SDI = 0.9–1.1 (Fig. 2c); Cu1 of hind wing complete; mid and hind trochantelli simple Enicospilus nigronotatus Cameron, 1903 without a decurved tooth; hind tarsal claw simply pectinate, [New Japanese name: Nettai-hoshi-amebachi] and distal pecten without longer than true apex of claw. (Figs. 1b, 2b) Distribution. Australasian (Australia and Papua New Guinea) and Oriental (Brunei, China, India, Indonesia, Japan*, Enicospilus nigronotatus Cameron, 1903: 133. Lectotype: F, Philippines, Sri Lanka, Taiwan, and Thailand) regions (Yu et

November 30, 2016, JJSE 22 (2) 206 Shimizu, S. and K. Maeto al., 2012). *New record. (Hymenoptera: Ichneumonidae). Bulletin of the Taiwan Bionomics. The specimens were often collected in light Agricultural Research Institute, 13: 1–79. traps (see Specimens examined). Crocidolomia pavonana Gauld, I. D., 1977. A revision of the Ophioninae (Hymenoptera: Ichneumonidae) of Australia. Australian Journal of Zoology (Fabricius) (Crambidae), fraterna (Moore) and (Supplementary Series), 49: 1–112. Euproctis scintillans (Walker) (), and Hypena Gauld, I. D., 1985. The phylogeny, classification and evolution of laceratalis Walker and Pericallia ricini Fabricius (Noctuidae) parasitic wasps of the subfamily Ophioninae (Ichneumonidae). are known as hosts (Yu et al., 2012). Bulletin of the British Museum of Natural History (Entomo- Remarks. This species is widely distributed in the logical Division), 51: 61–185. Australasian and Oriental regions. In Japan, it is found only in Gauld, I. D., 1988. A survey of the Ophioninae (Hymenoptera: the Ryukyu Islands (see Specimens examined). Ichneumonidae) of tropical Mesoamerica with special According to Gauld & Mitchell (1981), this is the commonest reference to the fauna of Costa Rica. Bulletin of the British Museum (Natural History), Entomology series, 57: 1–309. species in the E. xanthocephalus species-group, which is Gauld, I. D., 1991. The Ichneumonidae of Costa Rica, 1. Memoirs predominantly found in the Melanesian region and contains the of the American Entomological Institute, 47: 1–589. following eight species: E. xanthocephalus, E. lacteus Gauld Gauld, I. D. & T. Huddleston, 1976. The nocturnal Ichneumonoidea & Mitchell, 1981, E. charus Gauld & Mitchell, 1981, E. susu of the British Isles, including a key to genera. Entomologist's Gauld & Mitchell, 1981, E. pionus Gauld & Mitchell, 1981, Gazette, 27: 35–49. E. miscophus Gauld & Mitchell, 1981, E. sedlaceki Gauld & Gauld, I. D. & P. A. Mitchell, 1978. The taxonomy, distribution and Mitchell, 1981, and E. zeus Gauld & Mitchell, 1981. host preferences of African parasitic wasps of the subfamily Ophioninae. CAB: Slough. Commonwealth Institute of Specimens examined. JAPAN: 1M, Nishiamuro, Entomology, London. 287 pp. Kakeromajima Is., Amami IsIs., Kagoshima Pref., 7. VI. 2016, Gauld, I. D. & P. A. Mitchell, 1981. The taxonomy, distribution H. Yoshitake leg. (LT) (NIAES); 1M, Akazaki Park, Asani, and host preferences of Indo-Papuan parasitic wasps of Naze, Amami-ôshima Is., Kagoshima Pref., 18. VI. 2016, the subfamily Ophioninae. CAB: Slough. Commonwealth H. Yoshitake leg. (LT) (NIAES); 1F, Sueyoshi Park, Naha Institute of Entomology, London, 611 pp. City, Okinawa Is., Okinawa Pref., 30. VI. 2013, S. Fujie leg. Matsumura, S., 1912. Thousand of Japan. Supplement IV. (OMNH); 1M, Asato Pass, Asato, Naze, Amami City, Amami- Tokyo. 247 pp. ôshima Is., Kagoshima Pref. [28° 20` 32” N, 129° 30` 01” E; Nikam, P.K., 1975. Studies on Indian Ichneumonidae. Four new species of Enicospilus Stephens (Ophioninae) from 170 m alt.], 5–6. VII. 2014, S. Shimizu leg. (LT) (NIAES); Marathwada. Marathwada University Journal of Sciences, 14: 2FF, Ôkuni-rindô, Okuma, Kunigami Vil., Kunigami County, 193–202. Okinawa Is., Okinawa Pref. [26° 43` 38.7” N, 128° 12` 34.4” E; Nikam, P. K., 1980. Studies on Indian species of Enicospilus ca. 265 m alt.], 30. VI–1. VII. 2016, S. Shimizu et al. leg. (LT) Stephens (Hymenoptera: Ichneumonidae). Oriental Insects, (SEHU);1M, Nûha, Ôgimi Vil., Kunigami County, Okinawa 14: 131–219. Is., Okinawa Pref. [26° 41' 21.3" N, 128° 09' 01.3" E; ca. 200 Rousse, P., D. L. J. Quicke, C.A. Matthee, P. Lefeuvre & S. van m alt.], 29–30. VI. 2016, S Shimizu et al. leg. (LT) (KPMNH). Noort, 2016. A molecular and morphological reassessment of the phylogeny of the subfamily Ophioninae (Hymenoptera: Ichneumonidae). Zoological Journal of the Linnaean Society, Acknowledgements 178: 128–148. doi: 10.1111/zoj.12405 The authors would like to express sincere thanks to Dr. Shimizu, S., K. Watanabe & K. Maeto, 2016. Revision of the Taiwanese species of the genus Leptophion Cameron, Shin-ichi Yoshimatsu and Dr. Hiraku Yoshitake for their kind 1901 (Hymenoptera: Ichneumonidae: Ophioninae), with a support during the investigation at NIAES; to Dr. Chi-Feng discussion of their phenology and distribution. Zootaxa, 4144: Lee for his kind support at TARI; to Dr. Masahiro Ôhara 71–88. doi: 10.11646/zootaxa.4144.1.3 and Mr. Namiki Kikuchi (Hokkaido University) for their Short, M.W., S. Schmidt & M.J. Steinbauer, 2006. A key to kind support at SEHU; to Dr. Kazuhiko Konishi for his kind some Australian genera of large nocturnal Ichneumon-idae support at EUM; Mr. Shunpei Fujie (Osaka) for offering a (Hymenoptera), including flight periodicities and influence of valuable specimen; and Mr. Masato Ito (Kobe University) and moon phase on light trap catches. Australian Entomologist, Mr. Yôto Komeda (Kyushu University) for their kind help 33: 49–55. Shuckard, W.E., 1840. Ichneumonides. In: Swainson, W. & W.E. during field investigation in Okinawa Island. Shuckard 'The cabinet cyclopedia: on the history and natural arrangement of insects'. London. 406 pp. pp.185–187. References Stephens, J.L., 1835. Illustrations of British Entomology. Mandibulata 7. 312 pp. London. Broad, G.R. & M.R. Shaw, 2016. The British species of Enicospilus Stephens, J.F., 1845. Index, list of plates and errata of "Illustrations (Hymenoptera: Ichneumonidae: Ophioninae). European of British Entomology. Mandibulata. Vol. VII." Baldwin & Journal of Taxonomy, 187: 1–31. doi: 10.5852/ejt.2016.187 Cradock, London. 307–312 pp. Cameron, P., 1903. Descriptions of new genera and species of Szépligeti, G., 1906. Neue exotische Ichneumoniden aus der Hymenoptera taken by Mr. Robert Shelford at Sarawak, Sammlung des Ungarischen National Museums. Annales Borneo. Journal of the Straits Branch of the Royal Asiatic Musei Nationalis Hungarici, 4: 119–156. Society, 39: 89–181. Townes, H., 1971. The genera of Ichneumonidae, Part 4. Memoirs Cameron, P., 1905. On the phytophagous and parasitic Hymenoptera of the American Entomological Institute, 17: 1–372. collected by Mr. E.Green in Ceylon. Spolia Zeylanica, 3: Townes, H., M. Townes & V.K. Gupta, 1961. A catalogue and 67–143. reclassification of the Indo-Australian Ichneumonidae. Chiu, S.C., 1954. On some Enicospilus species from the Orient Memoirs of the American Entomological Institute, 1: 1–522.

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Uchida, T., 1928. Zweiter Beitrag zur Ichneumoniden-Fauna 20: 81–90. Japans. Journal of the Faculty of Agriculture, Hokkaido Yu, D. S., C. van Achterberg & K. Horstmann, 2012. Taxapad University, 21: 177–297. 2012, Ichneumonoidea 2011. Database on flash-drive. www. Watanabe, K. & T. Yamauchi, 2014. Records of ichenumonid taxapad.com, Ottawa, Ontario, Canada. wasps (Hymenoptera) from Yakushima Iskand, the Ryukyu Islands, Japan. Japanese Journal of Systematic Entomology, [Received: October 12, 2016; accepted: November 11, 2016]

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