First Records of the Pughead-Pipefish Bulbonaricus Davaoensis (Teleostei: Syngnathidae) from Japan

Species Diversity 25: 163–169 Published online 7 August 2020 DOI: 10.12782/specdiv.25.163

First Records of the Pughead-pipefish Bulbonaricus davaoensis (Teleostei: Syngnathidae) from Japan

Moeri Araki1, Kazutoshi Uehara2, Hiroshi Senou3, and Hiroyuki Motomura4,5 1 Graduate School of Agriculture, Forestry and Fisheries, Kagoshima University, 1-21-24 Korimoto, Kagoshima 890-8580, Japan 2 GT Divers Okinoerabu-jima, 471-3 Wadomari, Kagoshima 891-9112, Japan 3 Kanagawa Prefectural Museum of Natural History, 499 Iryuda, Odawara, Kanagawa 250-0031, Japan 4 The Kagoshima University Museum, 1-21-30 Korimoto, Kagoshima 890-0065, Japan E-mail: [email protected] 5 Corresponding author (Received 24 January 2020; Accepted 28 May 2020)

Five specimens (41.2–47.0 mm standard length) of the Indo-Pacific species Bulbonaricus davaoensis (Herald, 1953), previously recorded from Kenya, Taiwan, the Philippines, Indonesia, Papua New Guinea, Australia, and Fiji, were collected from Okinoerabu Island, Amami Islands, Ryukyu Islands and Chichi Island, Ogasawara Islands. The specimens represent the first Japanese and northernmost (Okinoerabu Island) records of the species. A detailed description is given for the specimens and the new standard Japanese name “Shuuyajiri-chin’yojiuo” is proposed for the species. Photographs of fresh metamorphosed adult specimens, a fresh larval specimen, and live individuals of B. davaoensis are provided. Key Words: distribution, Amami Islands, Ryukyu Islands, Ogasawara Islands.

pers under a dissecting microscope. Accurate counts and Introduction measurements of two specimens from Chichi Island were not possible due to the damaged tail tip; accordingly “+” The Indo-West Pacific genus Bulbonaricus Herald, 1953 was added to the counts and measurements taken. Stan- includes three valid species, B. brauni (Dawson and Allen, dard length is abbreviated as SL. Curatorial procedures for 1978), B. brucei Dawson, 1984, and B. davaoensis (Her- the KAUM specimens followed Motomura and Ishikawa ald, 1953) in which B. brauni has been previously recorded (2013). The following description was based solely on the five from Japan (Suzuki et al. 2002; Senou 2013; Koeda and Fujii Japanese specimens. The specimens and underwater photo- 2015). Bulbonaricus davaoensis, originally described as Ich- graphs examined are deposited at the Kagoshima University thyocampus davaoensis on the basis of a single non-meta- Museum, Kagoshima, Japan (KAUM–I. for specimens and morphosed planktonic specimen from Davao Gulf, Min- KAUM–II. for photographs) and the Kanagawa Prefectural danao, Philippines, has been subsequently recorded from Museum of Natural History, Odawara, Japan (KPM-NI and scattered localities in the Indo-West Pacific, the northern- KPM-NR, respectively). Comparative material of metamor- most record to date being Taiwan (Ho and Lin 2014). phosed adult B. brauni examined included: KAUM–I. 72147, During an ichthyofaunal survey of Okinoerabu Island, male, 40.1 mm SL, KAUM–I. 72148, female, 50.4 mm SL, off Amami Islands, Ryukyu Archipelago, three metamor- Atetsu, Setouchi, Amami-oshima Island, Amami Islands, phosed adult individuals of B. davaoensis were collected Kagoshima Prefecture, Japan, 28°10′51″N, 129°16′56″E, by the Kagoshima University Museum at a depth of 15 m 15 m depth, T. Fujii, 30 April 2015. in November 2019. In addition, two metamorphosed adult specimens collected from Chichi Island, Ogasawara Islands Bulbonaricus davaoensis (Herald, 1953) in January 2009 were recently found in the fish collection of [English name: Davao Pughead-pipefish; new standard the Kanagawa Prefectural Museum of Natural History. The Japanese name: Shuuyajiri-chin’yojiuo] combined five specimens, described here, represent the first (Figs 1–4; Table 1) and northernmost records of B. davaoensis from Japan. Ichthyocampus (Bulbonaricus) davaoensis Herald, 1953: 243, fig. 37 (type locality: Davao Gulf, Mindanao, Philippines). Materials and Methods Enchelyocampus sp.: Dawson 1980: 224, fig. 3 (Taam Island, Banda Sea, Indonesia). Counts and measurements followed Dawson (1977, Enchelyocampus brauni (non Dawson and Allen, 1978): 1984) and Allen and Erdmann (2008). Measurements were Dawson 1980: 225, fig. 4 (off Cape Melville, Cape York made to the nearest 0.1 mm with needle-point digital cali- Peninsula, Queensland, Australia).

Fig. 1. Photographs of fresh (A–C, F, G) and preserved (D, E, H, I) specimens of Bulbonaricus davaoensis from Japan, lateral views (A, B, D–I) and dorsal view (C). A–E: from Okinoerabu Island; F–I: from Chichi Island; A, D: KAUM–I. 134392, male, 41.2 mm SL; B, E: KAUM–I. 134391, female, 44.6 mm SL; C: KAUM–I. 134393, female, 47.0 mm SL; F, H: KPM-NI 23063, male, 44.1+mm SL; G, I: KPM-NI 23064, female, 40.9+mm SL.

Bulbonaricus davaoensis: Dawson 1984: 566, figs 1–3 (Ras Indonesia; Viti Levu Island, Fiji); Dawson 1985: 27, fig. 47 Iwatine, Mombasa, Kenya; Davao Gulf, Mindanao, Luzon (Ras Iwatine, Mombasa, Kenya; Davao Gulf, Mindanao, Island, Negros Island, the Philippines; Talisei Island, the Philippines; Talisei Island, Ambon Island, Moluccas Ambon Island, Moluccas and Taam Island, Banda Sea, and Taam Island, Banda Sea, Indonesia; off Cape Melville, First Japanese records of Bulbonaricus davaoensis 165

Table 1. Counts and measurements of specimens of Bulbonaricus davaoensis.

This study Herald (1953) Dawson (1984) Japan Philippines Indo-West Pacific Non- Non- Metamorphosed Metamorphosed specimens metamorphosed metamorphosed specimens specimen specimens KAUM–I. KAUM–I. KAUM–I. KPM-NI KPM-NI Holotype n=14** n=3 134391 134392 134393 23063 23064 Standard length 44.6 41.2 47.0 44.1+ 40.9+ 33 13.0–43.0 40–43 (SL; mm) Counts Trunk rings 18 16 16 17 17 16 16–17 Tail rings 45 43 45 35+ 32+ 43 40–45 Total rings 63 59 61 52+ 49+ 59 — Pectoral-fin rays — — — — — 11 9–13 — Dorsal-fin rays — — — — — 25 22–26 — Caudal-fin rays —* 10 —* — — 10 — — Subdorsal rings — — — — — 7.75 7.0–8.5 — Measurements (% of SL) Trunk length 24.2 22.3 25.3 — — 19.7 — — Tail length 67.7 69.7 69.8 — — 72.7 — — Head length 7.2 7.0 7.0 — — 7.6 — — Head width 2.2 2.4 2.1 — — — — — Snout length 1.1 1.5 1.1 — — 2.4 — — Orbital diameter 1.1 0.7 1.3 — — — — — Interorbital width 0.4 0.5 0.6 — — — — — Trunk width 2.1 1.9 1.7 — — — — — Trunk depth 4.0 3.6 4.0 — — — — — Anal ring depth 3.8 2.9 3.2 — — — — — Dorsal-fin base — — — — — 12.7 — — length Caudal-fin length 0.9 1.9 0.6 — — 4.5 — — Measurements — — — (% of HL) Trunk length 337.5 317.2 360.6 369.7 361.8 — — — Tail length 943.8 989.7 993.9 — — — — — Head length 100.0 100.0 100.0 100.0 100.0 — — — Head width 31.3 34.5 30.3 42.4 38.2 — — — Snout length 15.6 20.7 15.2 18.2 20.6 — — — Orbital diameter 15.6 10.3 18.2 18.2 11.8 — — — Interorbital width 6.3 6.9 9.1 9.1 11.8 — — — Trunk width 29.7 26.9 23.9 27.3 27.6 — — — Trunk depth 56.3 51.7 57.6 54.5 58.8 — — — Anal ring depth 53.1 41.4 45.5 48.5 55.9 — — — Caudal-fin length 12.5 27.6 9.1 — — — — — Posterior tip of tail in KPM-NI specimens damaged; *caudal fin present, but indistinct (poorly developed); **including holotype.

Cape York Peninsula, Queensland, Australia; Viti Levu Material examined. 5 specimens (2 males and 3 fe- Island, Fiji); Paxton and Hanley 1989: 413 (Great Bar- males) from Japan: KAUM–I. 134391, female, 44.6 mm SL, rier Reef, Queensland, Australia); Randall and Lim 2000: KAUM–I. 134392, male, 41.2 mm SL, KAUM–I. 134393, 603 (South China Sea); Allen and Adrim 2003: 27 (Papua female, 47.0 mm SL, 187 m off west of Tamina, China, New Guinea to Moluccas and North Sulawesi); Paxton et Okinoerabu Island, Amami Islands, Kagoshima Prefecture, al. 2006: 813 (Great Barrier Reef, Queensland, Australia); 27°22′49″N, 128°31′10″E, 15 m depth, K. Uehara, 16 No- Kuiter 2009: 290, unnumbered fig. (locality unknown); vember 2019; KPM-NI 23063, male, 44.1+mm SL, KPM- Allen and Erdmann 2012: 187, unnumbered fig. (off Cape NI 23064, female, 40.9+mm SL, Futami Bay, Chichi Island, Melville, Cape York Peninsula, Queensland, Australia); Ogasawara Islands, Tokyo, 27°05′N, 142°11′E, 6 m depth, O. Fricke et al. 2014: 45 (Madang, Papua New Guinea); Ho Morishita, 10 January 2009. and Lin 2014: 26, figs 1–3 (Kenting, Pingtung, Taiwan). Underwater photographs examined. All from Japan. 166 Moeri Araki et al.

Distribution. Bulbonaricus davaoensis has been recorded from Kenya (Ras Iwatine, Mombasa), Taiwan (Kent- ing, Pingtung), the Philippines (Davao Gulf, Mindanao), Indonesia (Talisei Island, Ambon Island, Moluccas; Taam Island, Banda Sea; and Liki Island, Irian Jaya), Papua New Guinea (Madang), Australia (off Cape Melville, Cape York Peninsula, Queensland), and Fiji (Viti Levu Island) (Her- ald 1953; Dawson 1984, 1985; Fricke et al. 2014; Ho and Lin 2014). The species is newly recorded from Okinoerabu Island (Amami Islands, Ryukyu Islands) and Chichi Island (Ogasawara Islands), Japan on the basis of voucher specimens, and Kakeroma Island (Amami Islands), Okinawa Is- Fig. 2. Diagram of lateral head of Bulbonaricus davaoensis. Same land (Okinawa Islands), Zamami Island (Kerama Islands), individual as Fig. 1A. Scale bar 1 mm. and Ishigaki Island (Yaeyama Islands), Ryukyu Islands, Japan on the basis of underwater photographs (this study). KPM-NR 97525, Nominoura, Oshima Strait, Kakeroma Remarks. Characters of the Japanese specimens agreed Island, Amami Islands, Ryukyu Islands, 5 m depth, 24 July well with those of the genus Bulbonaricus defined by Daw- 2008, photo by M. Kanazawa; KAUM–II. 83, Tamina, son (1984) and Suzuki et al. (2002), in having the following China, Okinoerabu Island, Amami Islands, Ryukyu Is- characters: superior trunk and tail ridges confluent; inferior lands, 27°22′49″N, 128°31′10″E, 15 m depth, 16 November trunk and tail ridges confluent; lateral trunk ridge straight; 2019, K. Uehara; KPM-NR 70435, Kitaya, Okinawa Island, trunk rings 16–18; total rings 59–63; anal fin absent; caudal- Okinawa Islands, Ryukyu Islands, 20 m depth, 11 Septem- fin rays 10 (in one specimen; counts in remaining specimens ber 2009, N. Shirakawa; KPM-NR 142824, Zamami Island, not available); head covered with fleshy integument, opercle Kerama Islands, Ryukyu Islands, 7.7 m depth, 11 November without distinct ridges, snout short and rounded, mouth in- 2013, H. Uchino; KPM-NR 92881, Nagura Bay, Ishigaki Is- ferior, both lips fleshy, and brood pouch on ventral surface land, Yaeyama Islands, Ryukyu Islands, 7 m depth, 6 May of tail in males (KAUM–I. 134392 and KPM-NI 23063). The 2007, T. Uchida; KPM-NR 95967, Ishigaki Island, Yaeyama following characters found in the Japanese specimens were Islands, Ryukyu Islands, 10 m depth, June 2006, Y. Yamada; consistent with diagnostic characters of B. davaoensis at the KPM-NR 97443, Futami Port, Chichi Island, Ogasawara metamorphosed adult stage, given by Dawson (1984): fron- Islands, 7 m depth, 1989, M. Satou; KPM-NR 97444, 97445, tal process rounded in cross section, spine-like, with smooth 97446, 206006, Futami Port, Chichi Island, Ogasawara dorsal margin; dorsal, pectoral and anal fins absent; a single Islands, 6 m depth, 5 January 2009, O. Morishita; KPM-NR white line on lateral surface of trunk; and scattered spots ab- 97448, Ogasawara Islands, 2009, O. Morishita. sent on head and body. By comparison, similar stage conge- Description. Counts and measurements given in Table 1. ners were characterized by scattered white spots on the head Head, including frontal process, illustrated in Fig. 2. Body and body (B. brauni) and the frontal process V-shaped, with elongate, slightly compressed. Body ridges smooth. Superior the dorsal margin spinose or denticulate (B. brauni and B. trunk and tail ridges continuous; lateral trunk ridge straight, brucei) (Dawson 1984; this study). Although Dawson (1984) ending at anal ring; inferior trunk and tail ridges continu- described B. davaoensis as having 16 or 17 trunk rings ous; median ventral trunk ridge indistinct. Head covered (based on examination of 17 specimens), KAUM–I. 134391 with fleshy integument. Snout very short, rounded; mouth (44.6 mm SL, Okinoerabu Island) had 18 trunk rings. inferior; both lips fleshy. Opercle without distinct ridges. Live coloration of B. davaoensis has been poorly known Frontal process rounded in cross section, spine-like, smooth to date. Although Allen and Erdmann (2012) stated “live on dorsal margin; brood pouch on ventral surface of first coloration unknown”, Dawson (1984) briefly described two to 20th (KPM-NI 230063) or 22nd (KAUM–I. 134392) tail African metamorphosed adult specimens as “pale pink rings in males; pectoral, dorsal, and anal fins absent; cau- color in smaller specimen and green in larger” (provided dal fin small in Okinoerabu Island specimens (KAUM–I. from collector). Subsequently, Ho and Lin (2014: figs 1–3) 134391–134393), lost in Chichi Island specimens (KPM-NI provided photographs of a dark red individual and a newly 23063, 23064) due to damaged tail. hatched larva. The present Japanese specimens were reddish Color when fresh (Fig. 1). Okinoerabu Island specimens: (Ryukyu Islands individuals, Fig. 3A) and greenish (Oga- body brownish-red dorsally, white ventrally. Dorsal surface sawara Islands individuals, Fig. 3B, C). Because the body of head greenish-red, with single white V-shaped mark an- sizes and morphology of these specimens were similar, with teriorly. Single deep red margin on ventral and posterior both sexes included in each color form, it is likely that color- edges of opercle in males; single white line on lateral sur- ation changes according to individual condition and/or host face of trunk, spots absent; base of brood pouch reddish- coral condition or species. Thus coloration differences are brown. Caudal fin white. Chichi Island specimens: body pale unlikely to represent species or population differences, al- brownish-white dorsally, white ventrally. Base of brood pouch though Dawson (1984) suspected that “more than one taxon brownish-orange. Single black margin on ventral and poste- may be included in Pacific Ocean material”. rior edges of opercle in males. Live color illustrated in Fig. 3. All of the Japanese specimens were collected from cavi- First Japanese records of Bulbonaricus davaoensis 167

Fig. 3. Underwater photographs of Bulbonaricus davaoensis from Japan. A: KAUM–II. 83, Okinoerabu Island, Amami Islands, 15 m depth, taken by K. Uehara (photographed individual was collected and registered as either KAUM–I. 134391, 134392, or 134393); B: KPM-NR 97444, Chichi Island, Ogasawara Islands, 6 m depth, taken by O. Morishita; C: same data as B. 168 Moeri Araki et al.

opted by the Ministry of Education, Culture, Sports, Science and Technology, Japan; and the “Island Research” project of Kagoshima University.

References

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