Biogeography 21. 12–16. Sep. 20, 2019

A new record of the exotic species Pithemera bicincta (Perrier, 1875) (Annelida: : ) from Japan

Masamichi T. ITO1*, Sayaka SATOH2, Motohiro HASEGAWA3, Kazuto KAWAKAMI4, and Yukio MINAMIYA5

1 Faculty of Economics and Management, Surugadai University 2 Mishima City Kita Elementary School 3 Department of Environmental Systems Science, Faculty of Science and Engineering, Doshisha University 4 Wildlife Ecology Laboratory, Forestry and Forest Products Research Institute 5 Tochigi Prefectural Museum

Abstract: We report the first unambiguous identification of the exotic earthworm species, Pithemera bicincta (Perrier, 1875) on Honshu, Shikoku, Kyushu, the Ogasawara Islands, and Ryukyu Islands, Japan. The species is redescribed in this paper based on the specimens from Shizuoka Pref., Honshu.

Key words: earthworm, Honshu, Japan, Megascolecidae, new record, Ogasawara Islands, Pithemera bicincta, Shikoku, Kyushu, Ryukyu Islands

Introduction lucida. We used the classification system from Sims and Easton The earthworm Pithemera bicincta originally was described (1972), mainly following their terminology, along with that of from specimens collected from the Philippines (Perrier, 1875). Ishizuka (1999) It is a known exotic species that is distributed in many tropi- cal or subtropical countries (Fragoso et al., 1999). Although Taxonomic Account Ohfuchi (1957) first reported it in Japan on Ishigakijima Island and Hatomajima Island, the accuracy of the record appears Family Megascolecidae Rosa, 1891 doubtful, because his description of P. bicincta does not cor- Genus Pithemera Sims & Easton, 1972 respond to those of Perrier (1875). Since then, no additional specimens have been recorded from Japan. Among the numer- Pithemera bicincta (Perrier, 1875) ous specimens of pheretimoids we collected during our studies (Fig. 1, Table 1) on Japanese , we provide the first unambiguous record of P. bicincta from Shizuoka, Pref., Honshu, Kochi Perichaeta bicincta Perrrier, 1875, p. 1044; Michaelsen, 1900, and Ehime Prefs. Shikoku, Oita Pref., Kyushu, the Ogasawara p. 419. Islands (Bonin Islands) and Ryukyu Islands. We also note that Megascolex bicinctus: Vaillant, 1889, p. 83. the original description of this species is insufficient for its violacea Beddard, 1895, p. 407; Cognetti de Marti- identification and thus provide a complete redescription with is, 1905, p. 34; Michaelsen, 1916, p. 15. fine drawings that include internal characters. Amyntas bicinctus: Beddard, 1900, p. 651. Pheretima bicincta: Stephenson, 1916, p. 335; Michaelsen, Methods 1922, p. 23; Stephenson, 1923, p. 294; Gates, 1937a, p. 195; 1937b, p. 346; 1942, p. 91; 1963, p. 12; 1982, p. 40; Earthworms were collected by hand from litter and/or soil Standen, 1988, p. 46; Fragoso, Kanyonyo, Moreno, Senapa- and transported to the laboratory within 6 h. Worms were ti, Blanchart & Rodriguez, 1999, p. 7, Table 1.1. anesthetized and killed in ethanol and fixed in formaldehyde Pheretima (Pheretima) bicincta: Michaelsen, 1935, p. 107. within 10 h. Fixed specimens were observed with stereoscopic Pithemera bicincta: Sims & Easton, 1972, p. 232; Lee. 1981, p. microscopes (NIKON SMZ-10) and illustrated with a camera 563; Easton, 1982, p. 732; Nakamura, M., 1990, p. 102; Ta- −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−− lavera, 1990, p. 162; Reynolds, 1994, p. 137; Shih, Chang & *Corresponding author: Faculty of Economics and Management, Suru- gadai University, 698 Azu, Hanno, Saitama, 357-8555 Japan; Chen, 1999, p. 438; Nakamura, Y., 1999, p. 18; Tsai, Shen e-mail: [email protected] & Tsai, 2000, p. 288; James, 2004, p. 12, fig. 7; Blakemore,

– 12 – Masamichi T. ITO, Sayaka SATOH, Motohiro HASEGAWA, Kazuto KAWAKAMI and Yukio MINAMIYA

2004a, p. 133, Table 1; Blakemore, Chang, Chuang, Ito, alt. 58 m a.s.l., 27.117998N, 142.1682957E, Nishijima, Oga- James & Chen, 2006, p. 230; Blakemore, Ito & Kaneko, sawara-mura, Tokyo Metropolitan, 17 June 2012, M. Haseg- 2006, p. 179; Reynolds, 2009, p. 59; Tsai, Shen, Tsai, Lin, awa coll.; 1 specimen (No. 8), forest of Livistona chinensis Hsieh & Yo, 2009, p. 38; Csuzdi & Pavlíček, 2009, p. 12; var. boninensis without Casuarina equisetifolia alt. 68 m a.s.l., Chang, Shen & Chen, 2009, p.142; Reynolds, 2010, p. 152; 27.1163529N, 142.1686496E, Nishijima, Ogasawara-mura, 2011, p. 283; 2015, p. 118; Xiao, 2019, p. 342. Tokyo Metropolitan, 17 June 2012, M. Hasegawa coll.; 2 Pithemera violacea: Sims & Easton, 1972, p. 232. specimens (Nos. 9–10), coastal glassland of Arundo donax and Peretima bicincta [sic]: Standen, 1988, p. 44, Table 3. Miscanthus sinensis alt. 5 m a.s.l., 33.107320N, 132.322731E, Oitsukamijima Island, Hiburishima, Uwajima-shi, Ehime Material examined. Six specimens (Nos. 1–6), arboretum Pref., 5 June 2010, Y. Minamiya and K. Ohga coll.; 3 speci- of mandarin orange grove, alt. 12 m a.s.l., 34.63997222N, 138. mens (Nos. 11–13), road side along evergreen broad-leaved 89019444E, Minato, Minamiizu-cho, Shizuoka Pref., 9 Octo- forest, alt. 170 m a.s.l., 32.735069N, 132.561528E, Okinoshi- ber 2011, S. Satoh coll.; 1 specimen (No. 7), forest of Livisto- ma, Okinoshima-machi, Sukumo-shi, Kochi Pref., 23 Feb. na chinensis var. boninensis including Casuarina equisetifolia, 2008, Y. Minamiya coll.; 4 specimens (Nos. 14–17), road

Fig. 1. Pithemera bicincta (Perrier, 1875), specimen No. 1. A, ventral view of anterior body; B, spermathecal pores in furrows 4/5/6/7/8/9; C, male pore in segment 18; D, spermatheca; E, prostate gland; F, intestinal caeca. Specimen number corresponds to that used in the text and Table 1, and all scale bars indicate 1 mm.

– 13 – New record of P. bicincta from Japan

Table1. Measurements (mm) of 26 specimens of Pithemera bicincta (Perrier, 1875) from Japan, examined in this study. Specimen numbers correspond to those used in the text.

Locality and Specimen Body length Body width Segments number No.1 80.0 2.7 95 No.2 84.0 2.3 85 No.3 58.0 2.0 61 Shizuoka Pref. (Minamiizu) No.4 86.0 2.4 95 No.5 77.0 2.0 89 No.6 64.0 1.9 66 No.7 65.8 3.1 107 Tokyo Pref. (Ogasawara) No.8 61.7 2.5 101 Ehime Pref. (Oitsukamijima) No.10 59.9 2.7 78 No.11 52 2.1 95 No.14 60.1 3.2 83 No.15 57.8 3 78 Kochi Pref. (Okinoshima) No.16 56.2 3.1 86 No.17 51.7 2.7 86 No.18 60.9 2.6 78 No.19 85.5 2.9 90 Oita Pref. (Usuki) No.20 68.7 2.7 74 No.22 73.4 3.3 88 No.23 72 3.3 94 No.24 68.9 3 83 No.25 68 3.1 88 Okinawa Pref. (Higashi) No.26 65.4 2.9 91 No.27 64.6 3.1 88 No.28 63.7 3.2 86 No.29 57.7 3.1 77 No.30 49.5 3.2 90 side along glassland of Arundo donax and Miscanthus sinen- and frontal 1/3 part of segment 16. Female pores duplicate. sis, alt. 50 m a.s.l., 32.718817N, 132.550929E, Okinoshima, Male pores simple and superficial on segment 18. Intestinal Okinoshima-machi, Sukumo-shi, Kouchi Pref., 27 Sept. caeca in segment 22, simple type. Prostate gland extending 2008 Y. Minamiya, K. Ohga and T. Fukuda coll.; 1 specimen through segments 18–20. (No. 18), road side along forest of Quercus phillyraeoides, alt. 72 m a.s.l., 32.731687N, 132.545657E, Okinoshima, Descripition Okinoshima-machi, Sukumo-shi, Kochi Pref., 16 May 2010 Measurements. Body length 51.7–86.0 mm, body width of Y, Minamiya and K. Ohga coll.; 2 specimens (Nos. 19–20), segment 13 1.9–3.2 mm (Table 1). road side along evergreen broad-leaved forest, alt. 2 m a.s.l., External characters. Color in formalin: grayish brown; 33.123374 N, 131.857855 E, Tsuboe, Fukae, Usuki-shi, Oita clitellum brown. Prostomium epilobous. Numbers of segments Pref., 25 June 2010, Y. Minamiya, K. Ohga and Y. Kumekawa 61–107 (Table 1). Clitellum segments 14–15 and frontal 1/3 coll.; 1 specimen (No. 21), soil around the building of Yona part of segment 16 with no setae. Dorsal pores beginning in Field, University of the Ryukyus, alt 10 m a.s.l., 26.763146N, furrow 11/12. Arrangement of setae perichaetine. Female 128.215739E, Yona, Kunigami-son, Okinawa Pref., 25 May pores duplicate, located mid-ventrally in segment 14. Preclitel- 2008, Y. Minamiya coll.; 14 specimens (Nos. 22–35), road lar and postclitellar genital markings absent. Male pore simple side along evergreen broad-leaved forest, alt. 111 m a.s.l., but hardly visible, on medium-sized circular porophores, su- 26.644811N, 128.186661E, Kawata, Higashi-son, Okinawa perficial on segment 18 (Fig. 1C). Five pairs of spermathecal Pref., 29 May 2008, Y. Minamiya coll. pores in furrows 4/5/6/7/8/9 (Fig. 1B). Internal characters. Five pairs of spermathecae in seg- Diagnosis. Five pairs of spermathecal pores in furrows ments 5–9 (Fig. 1D). No nephridia associated with spermath- 4/5/6/7/8/9. Five pairs of spermathecae in segments 5–9 with ecal ducts. Spermatheca developed as shovel-shaped ampulla no nephridia on spermathecal duct. Clitellum segments 14–15 with convoluted diverticulum. Genital gland absent. Seminal

– 14 – Masamichi T. ITO, Sayaka SATOH, Motohiro HASEGAWA, Kazuto KAWAKAMI and Yukio MINAMIYA vesicles small extending into segments 10 and 11. Prostate the exotic lumbricids Eisenia fetida and Eiseniella tetrae- gland extending through segments 18–20 (Fig. 1E). Simple dra. Taiwania, 51 (3): 226-236. intestinal caeca, originating in segment 22 (Fig. 1F). Blakemore, R. J., Ito, M. T. & Kaneko, N., 2006. Alien earth- Remarks. In 1957, Ohfuchi reported the first occurrence of worms in the Asia/Pacific region with a checklist of species Pheretima bicincta on Ishigakijima Island and Hatomajima Is- and the first records of Eukerria saltensis (Oligochaeta: land, Japan. Ohfuchi noted it had intestinal caeca in segments Ocnerodrilidae) and Eiseniella teteraedra (Lumbricidae) 26 or 27. However, this finding should place the specimen from Japan, and Pontoscolex corethrurus (Glossocolecidae) in either genera Amynthas or Begemius and not P. bicincta. from Okinawa. In: Koike, F., Clout, M. N., Kawamichi, M., Unfortunately, it is impossible to evaluate Ohfuchi’s speci- De Poorter, M., Iwatsuki, K. (eds.) Assessment and control mens because they were lost. Therefore, we cannot confirm of biological invasion risks, pp. 173-181. Shoukadoh Book his reports of P. bicincta in Japan and thus exclude the fol- Sellers, Kyoto, Japan. lowing records of the species that are dependent on Ohfuchi’s Chang, C., Shen, H. & Chen, J., 2009. Earthworm Fauna of record; Kamihira, 1973, Easton, 1981, Ishizuka, 1999, 2000, Taiwan. National Taiwan University Press, Taipei, Taiwan. Blakemore, 2003, 2004b, 2012. Cognetti de Martiis, L., 1905. Gli Oligocheti della regione According to the location data in this paper, as well as Neotropicale. Mem. Real. Accad. Sci. Torino, 56: 1-72, figs. our redescription, we conclude that P. bicincta is distributed 1-38. broadly across Southwest Japan including the Ryukyu Islands. Csuzdi, C. & Pavlíček, T., 2009. 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