Phasmida: Phasmatidae)

Zootaxa 4941 (4): 587–593 ISSN 1175-5326 (print edition) https://www.mapress.com/j/zt/ Correspondence ZOOTAXA Copyright © 2021 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4941.4.8 http://zoobank.org/urn:lsid:zoobank.org:pub:073AFF56-749C-49C5-84CA-2F431A0AD1B4

Studies on Ramulus ussurianus (Bey-Bienko, 1960) (Phasmida: Phasmatidae)

SERGEY YU. STOROZHENKO1 & TAEWOO KIM2 1Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivo- stok, 690022, Russia. �[email protected]; https://orcid.org/0000-0001-9269-4043 2National Institute of Biological Resources, Hwangyeong-no 42, Seo-gu, Incheon, 22689, South Korea. �[email protected]; https://orcid.org/0000-0002-3387-6370

The phasmid genus Ramulus Saussure, 1862 belongs to the nominotypical tribe of subfamily Clitumninae of the Phas- matidae. This genus consists of 159 species distributed in India (21 species), Sri Lanka (6 species), Bhutan (1 species), Myanmar (6 species), Thailand (1 species), Vietnam (12 species), Malaysia (4 species from Peninsular part and Borneo), Indonesia (18 species from Java, Sumatra, Borneo, Sulawesi, and Key islands), the Philippines (3 species), China includ- ing Taiwan (74 species), Japan (1 species), Korea (1 species), and Russia (1 species) (Brock et al., 2021). Three phasmid species have been described in the genus Baculum Saussure, 1861 from the Russian Far East, Korea and North-East China respectively (Bey-Bienko, 1960; Kwon et al., 1992; Chen & He, 1994) and later transferred to the genus Ramulus (Otte & Brock, 2005). As a result of detailed examination of the type specimens of Ramulus ussurianus (Bey-Bienko, 1960), additional material and descriptions of these species, it became clear that specimens from Russia, Korea and North-East China are conspecific.

Material and methods The present study is based on the collections of the Zoological Institute of the Russian Academy of Sciences, St. Peters- burg, Russia (ZIN), the Federal Scientific Center of the East Asia Terrestrial Biodiversity, Vladivostok, Russia (FSCB), and the National Institute of Biological Resources, Incheon, Korea (NIBR), as well as on the critical analysis of published data. The morphological terminology followed those of Bragg (1997) and terminology for the egg follows Clark Sellick (1997). Photographs of egg were taken with an Olympus SZX16 stereomicroscope and an Olympus DP74 digital camera, and then stacked using Helicon Focus software. The final illustrations were post-processed for contrast and brightness using Adobe® Photoshop® software. Black and white drawings were made under a MBS-10 stereomicroscope.

Family Phasmatidae Leach, 1815 Ramulus ussurianus (Bey-Bienko, 1960) (Figs 1–15) Baculum ussurianum Bey-Bienko, 1960: 690, fig. 1 (holotype—female, Russia: Primorskii krai, “middle stretch of Daubikhe River, Anuchinskii district” [= Arsenyevka River, vicinity of Vinogradovka village, 43°45ʹ N, 132°57ʹ E]; deposited in the Zoological Institute of the Russian Academy of Sciences, Russia); Sinchilina, 1972: 154; Storozhenko, 1986: 240, fig. 113; Perepelkina & Veriga, 2005: 62. Ramulus ussurianus: Otte & Brock, 2005: 307; Brock, 2007: 55. Baculum koreanus Kwon, Ha & Lee, 1992: 50, 51, fig. 3, Pl. 3A-G (holotype—female, Korea: “Kyonpuk Prov., Chuwangsan” [= Mt. Juwangsan, Cheongsong-gun, Gyeongsangbuk-do, 36°23ʹ N, 129°10ʹ E]; deposited in the Kyungpook National University, Daegu, Republic of Korea); syn. nov. Ramulus koreanus: Otte & Brock, 2005: 307. Baculum minutidentatum Chen & He, 1994: 197, figs. 3, 4 (holotype—female, China: ‘Liaoning Province, Huanren Co.” [= Huanren Manchu Autonomous County, 41°16ʹ N, 125°21ʹ E]; deposited in the Beijing Forestry University, Beijing, China]; syn. nov. Baculum minutidentatum: Wang & Zhou, 2003: 31; Chen & He, 2008: 288, fig. 253. Ramulus minutidentatus: Otte & Brock, 2005: 304; Hennemann et al., 2008: 31, 50. Type material examined. Russia. Primorskii krai: Anuchinskii district, vicinity of Vinogradovka village, 28-30 Au- gust 1957, 2 ♀ (holotype and paratype), leg. E.S. Sinchilina (ZIN).

Accepted by B. Mantovani: 19 Feb. 2021; published: 10 Mar. 2021 587 Other material examined. Russia. Spasskii district, vicinity of Tatyanovka village, 12 August 1960, 4 ♀, leg. E.S. Sinchilina; the same locality, 12 August 1965, 14 ♀, leg. N.A. Krylov; Spasskii district, vicinity of Dubovskoe village, 20-30 August 1996, 13 ♀, leg. M.A. Koshcheev; Chernigovskii district, 10 km SE Chernigovka, vicinity of Gribnoe village, 29 July 1996, 1 ♀ (nymph), leg. S.A. Belokobylskij; Anuchinskii district, 30 km NW Arseniev city, 9 October 2002, 12 ♀, leg. S.V. Veriga; the same locality, 10 August 2004, 98 ♀, 1 ♂, leg. S.A. Veriga and other local collectors (FSCB). Republic of Korea. Gangwon-do: Baekdamsa Temple, Mt. Seolaksan, Buk-myeon, Inje-gun, 27 June 2015, 3 ♀ (nymphs), leg. Kim Taewoo; Jeohangryeong, Mt. Seolaksan, Sokcho-si, 22 July 2004, 1 ♀ (nymph), leg. JK Kim; Gotoil-gil, Gonhan-eup, Jeongseon-gun, 4 September 2015, 2 ♀, leg. Kang Euyong & Oh Heungyun; Mt. Gariwan- gsan, Hoedong-ri, Jeongseon-eup, Jeongseon-gun, 2 September, 2009, 1 ♀ (sweeping), leg. WY Choi, OS Kim, & YW Lee; Mt. Chiaksan, Wonju-si, 19 July 1998, 1 ♀, leg. Kim Seong-A; Chungcheongbuk-do: Miwon-ri, Miwon-myeon, Cheongwon-gun, 22 July 2013, 1 ♀ (nymph), Kim In-Hee; Mt. Wolaksan, Jecheon-si, 13 August 1987, 1 ♀, collector unknown; Gyeongsangbuk-do: Jukgye, Sunheung-myeon, Yeongju-si, 21 July 2008, 1 ♀, leg. Lee Jongwook; Abgokam Temple, Mt. Seonamsan, Gaap-ri, Goro-myeon, Gunwi-myeon, 20 July 1998, 2 ♀, leg. An Taeho & An Namyoung; Mt. Geumosan, Gumi, 19-20 July 2001, 1 ♀, leg. Kim Jin-ill & Kim A-yong; Huibangsa Temple, Mt. Sobaeksan, Yeongju-si, 2 August 1994, 2 ♀, leg. Moon Tae-Young; Gyeongsangnam-do: Icheon-ri, Sangbuk-myeon, Ulsan-si, 6-8 August 1992, 1 ♀, collector unknown; Hansin-gyegok, Chuseong-ri, Macheon-myeon, Hamyang-gun, 29-30 July 1992, 1 ♀, collector unknown; Mt. Jirisan, Jungsan-ri, Sicheon-myeon, Sancheong-gun, 12 August 2010, 1 ♀, leg. Kim Taewoo (NIBR). Description. Female. Body smooth, medium size for the genus. Apterous. There are two color forms: green (Fig. 2) and brown (Fig. 1); the former is most common (about 95 % of studied specimens). Head prognathous (Fig. 7), slightly extended, longer than pronotum (Fig. 4). Vertex without granules or transverse ridge between compound eyes. Occiput and genae smooth. Compound eyes oval, prominent. Antennae 21–22-segmented, 2.7–2.8 times shorter than fore femora; scapus flat and broad, about three times length of pedicel, other segments cylindrical, 3rd segment longest. Pronotum elongated, slightly expanded posteriorly, anterior margin concave, posterior margin truncate, transverse and longitudinal sulci crossing at the middle (Fig. 4). Mesonotum and metanotum smooth, with distinct median carina. Mesonotum longer than metanotum and median segment combined. Median segment shorter than tergite II. Mesopleurae and metapleurae smooth. Abdomen cylindrical, smooth, dorsally with vestigial median carina. The length of tergites III-VII almost equal. Tergite VIII distinctly longer than tergite IX (Fig. 6). Tergite X (= anal segment) relatively narrow, apically with two lateral lobes and a short anal plate between them (Fig. 5). Sternite VII without praeopercular organ. Operculum (= sternite VIII; subgenital plate) reaching apex of tergite X; laterally boat-shaped (Fig. 6); ventrally with distinct median carina in apical third of sternite. Cerci short, cylindrical, not reaching posterior margin of the tergite X. Fore femora curved basally, shorter than fore tibiae. Mid femora and mid tibiae approximately equal length; hind femora shorter than hind tibiae. All femora dorsally unarmed, ventrally with short apical carinula armed by 3–4 small blackish teeth. Male (first description). Similar to female but smaller and slender. Body smooth, light brown with black lateral stripes along thorax and abdomen (Fig. 3). Head longer than wide and 1.1 times longer than pronotum; dorsum of head without depressions between bases of antennae and spines between eyes; vertex, occiput and genae smooth. Compound eyes oval, prominent. Antennae 22-segmented, 1.4 times shorter than fore femora; scapus elongated, slightly flat, about two times length of pedicel, other segments cylindrical, almost equal. Pronotum distinctly expanded posteriorly, elongated; anterior margin concave, posterior margin truncate, lateral margins S-shaped; transverse and longitudinal sulci as in female. Mesonotum and metanotum smooth, without median carina. Mesonotum 1.2 times longer than metanotum and median segment combined. Median segment 1.7 times shorter than tergite II. Mesopleurae and metapleurae smooth. Abdomen narrow, cylindrical, smooth. The length of tergites II-III almost equal; tergites IV-VII slightly longer. Tergite VIII and IX short, widened (Fig. 8). Tergite X (= anal segment) as long as tergite IX, dilated into two distinct lobes, tapering posteriorly. Inner margins of lobes curved inwards, with more than 10 irregularly arranged blackish teeth and numerous short setae (Figs. 9, 10). Posterior margin of the last sternite triangularly concave. Poculum laterally boat-shaped, not reaching the apex of tergite IX (Fig. 9), ventrally shallow concave at apex. Cerci short, cylindrical, not reaching posterior margin of tergite X (Fig. 10). Fore femora curved basally, dorsally and ventrally unarmed, 1.4 times shorter than fore tibiae. Mid femora and mid tibiae distinctly shorter than fore ones. Hind hind femora shorter than hind tibiae. Mid and hind femora ventrally with short apical carinula armed by 2–3 small blackish teeth. Measurements. Lengths (in mm). Body: ♀ 75.0–90.0, ♂ 57.0; head: ♀ 4.2–4.5, ♂ 2.8; antenna: ♀ 8.7–9.1, ♂ 19.5; pronotum: ♀ 2.8–3.0, ♂ 2.5; mesonotum: ♀ 13.7–16.5, ♂ 12.7; metanotum: ♀ 9.5–10.3, ♂ 8.4; median segment: ♀ 2.0–2.5, ♂ 2.1; abdomen: ♀ 45.0–51.0, ♂ 35.0; fore femur: ♀ 23.5–25.0, ♂ 26.5; fore tibia: ♀ 27.5–29.0, ♂ 37.2; mid femur: ♀ 14.3-15.5, ♂ 16.5; mid tibia: ♀ 14.9-16.3, ♂ 19.7; hind femur: ♀ 18.0–20.0, ♂ 20.5; hind tibia: ♀ 19.5-20.4, ♂ 18.0; cercus: ♀ 0.9–1.0, ♂ 1.0.

588 · Zootaxa 4941 (4) © 2021 Magnolia Press STOROZHENKO & KIM Figures 1–3. Ramulus ussurianus, adult in nature and holding cage (Primorskii krai, Russia). 1. Female (brown form); 2. Female (green form) and male before copulation; 3. Male. (S. Veriga).

Figures 4–7. Ramulus ussurianus, female (4, 5—after Bey-Bienko, 1960; 6, 7—after Storozhenko, 1986). 4. Head and pronotum, dorsal view; 5. Apex of abdomen, dorsal view; 6. The same, lateral view; 7. Head, lateral view. (Cer—cercus; Op—operculum; Tg- 8–Tg-10—abdominal tergites VIII–X respectively).

Studies on Ramulus ussurianus Zootaxa 4941 (4) © 2021 Magnolia Press · 589 Egg. Capsule length 3.4–3.5 mm, width 1.1–1.2 mm, height 1.6–1.7 mm. Capsule generally flattened and slightly concave; surface matt, grey to dark brown; ventral and dorsal sides with a pair of longitudinal ridges (Figs. 11, 12). Capitulum absent. Operculum broadly oval with numerous irregular short ridges (Fig. 13). Micropylar plate elliptical; micropyle situated almost in the central part of plate (Fig. 14). The eggs described herein from Russia appear to be identi- cal to figured ones from China (Chen & Li, 1999) and Korea (Kwon et al., 1992), further supporting the proposed new synonymy. Notes. Ramulus ussurianus was described by two females which Brock (2007: 55) considered as syntypes. This is incorrect because Bey-Bienko (1960: 691) discussed variability of his new species and compared the type (marked by golden circle) with paratype (without circle); therefore the type series consists of holotype and paratype (Fig. 15). Biology. The nocturnal Ramulus ussurianus is known as a parthenogenetic species overwintering in the egg stage. Development takes place through four nymphal instars: 1st (body length 10–15 mm), 2nd (17–28), 3rd (28–35), and 4th (40–70 mm) (Perepelkina & Veriga, 2005). In nature the nymphs hatch from late May while adults are observed from late July to the early November. The maximum density of immature and adult Ramulus ussurianus in Russia is a reported 30–45 specimens per m2 (Perepelkina & Veriga, 2005) while in China (Tongua city, Jilin province) 2000–5000 insects were scored on a single Tilia mandshurica tree (Wang & Zhou, 2003). The density of dropped eggs was 500–600 per m2 in Russia and 1000–3000 per m2 in China, each female laying 180–280 eggs. The first and only one male so far collected and here described has been found in Primorskii krai in 2004 together with thousands of females collected at the same locality and time. A copulation lasting 10 minutes was observed on 17 August 2004; male takes position above the female and the heads of both sexes are directed in the same direction (Pere- pelkina & Veriga, 2005).

Figures 8–10. Ramulus ussurianus, male. 8. Apex of abdomen, dorsal view; 9. The same, lateral view; 10. The same, ventral view. (Cer—cercus; Poc—poculum; St-8–St-9—abdominal sternites VIII and IX respectively; Tg-8–Tg-10—abdominal tergites VIII–X respectively).

590 · Zootaxa 4941 (4) © 2021 Magnolia Press STOROZHENKO & KIM Figures 11–14. Ramulus ussurianus, egg from Primorskii krai (Russia). 11. Capsule, lateral view; 12. The same, dorsal view; 13. Operculum. 14. Micropylar plate.

Food plants. The main food plants are Betula dahurica Pall., B. mandshurica (Rgl.) Nakai (Betulaceae), Ulmus propinqua Koidz. (Ulmaceae), Acer tegmentosum Maxim., A. mandshuricum Maxim., A. mono Maxim. (Sapindaceae), Filipendula palmata Maxim. (Rosaceae), Tilia amurensis Rupr., T. mandshurica Rupr. et Maxim. (Malvaceae), while the leaves of Actindia arguta (Sieb. et Zucc.) Planch. (Actinidiaceae), Euonymus sp. (Celastraceae), Quercus mongolica Fisch. (Fagaceae), Lonicera maackii Rupr., Weigela subsessilis Bail. (Caprifoliaceae), Salix caprea L. (Salicaceae), Ul- mus laciniata (Trautv.) Mayr., Zelkova serrata (Thunb.) Mak. (Ulmaceae), Carpesium macrocephalum Franch. et Sav. (Asteraceae), Acer barbinerve Maxim. (Sapindaceae), Arctium lappa L. (Asteraceae), Corylus mandshuricum Maxim. et Rupr. (Betulaceae), and Fraxinus mandshurica Rupr. (Oleaceae) are also used (Sinchilina, 1961, 1972; Kwon et al., 1992; Wang & Zhou, 2003; Perepelkina & Veriga, 2005). Pest status. In Russian Far East (Primorskii krai) this species is known as a serious pest, badly defoliating forests in several districts in 1959 and 2002–2004 (Sinchilina, 1972; Perepelkina & Veriga, 2005). All younger trees and bushes were killed and bigger trees became dry and withered. In 1991 and 1998–2001 similar serious damage occurred in Jilin province, China (Xu et al., 1994; Wang & Zhou, 2003). Distribution. China (Liaoning and Jilin provinces), Korea (Gangwon-do, Gyeonggi-do, Chungcheongbuk-do, Gyeongsangbuk-do, Gyeongsangnam-do and Jeollabuk-do), and Russia (Primorskii krai).

592 · Zootaxa 4941 (4) © 2021 Magnolia Press STOROZHENKO & KIM Acknowledgements We thank Dr. A.V. Gorochov for the possibility to study the collections of the Zoological Institute (St. Petersburg), to Dr. V.M. Loktionov (Federal Scientific Center of the East Asia Terrestrial Biodiversity, Vladivostok) for his assistance in preparing photographs of egg, and S.V. Veriga (Vladivostok) for providing the adult photos. This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR201907101). Two anonymous reviewers kindly commented on earlier drafts of the manu- script.

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