Notes on the occurrence of Orthoprotella spinigera Mori, 1996 (Crustacea: Amphipoda: Caprellidae) from Okinawa Island, Japan

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1 Plankton Benthos Res 9(2): , 2014 Note Plankton & Benthos Research The Japanese Association of Benthology Notes on the occurrence of Orthoprotella spinigera Mori, 1996 (Crustacea: Amphipoda: Caprellidae) from Okinawa Island, Japan ICHIRO TAKEUCHI* & YUKI INOUE Department of Life Environment Conservation, Faculty of Agriculture, Ehime University, Tarumi, Matsuyama, Ehime , Japan Received 24 September 2013; Accepted 17 March 2014 Abstract: Orthoprotella spinigera Mori, 1996 (Crustacea: Amphipoda: Caprellidae) was collected from a coral reef at Oura Bay on the east coast of Okinawa Island, Japan. This is only the second record for O. spinigera. The type locality is the Amakusa Islands, Kyushu, ca. 700 km north of the current collection. The species may be widely distributed along the western and southern coasts of Japan. Orthoprotella spinigera appears similar to Metaprotella sandalensis Mayer, 1898, but differs in the head having a pair of apical rounded projections, lacking a triangular projection below the eye, and having longer fused pereonites 6 and 7. Key words: Amphipoda, coral reef, Orthoprotella spinigera, Okinawa, Japan SCUBA surveys by the diving team Snack Snufkin documenting coral reef community diversity at Oura Bay on the east coast of Okinawa Island, Japan, collected 4 large male Caprellidae. These specimens appeared similar to Metaprotella sandalensis Mayer, 1898, which is widely distributed in shallow waters of the tropical Indo-West Pacific coasts (see Mayer 1898, 1903, McCain & Steinberg 1970, Müller 1990, Laubitz 1991, Lim & Takeuchi 2012). However, closer inspection of these specimens revealed that they are Orthoprotella spinigera Mori, 1996, previously known only from Tomioka, Amakusa Islands, on the west coast of Kyushu. Herein, is provided a detailed description of O. spinigera from Okinawa Island. The described specimen was dissected under a binocular microscope. Gnathopod 1, pereopods 5 to 7 and mouthparts were mounted onto slides in polyvinyl-lactophenol. The lateral body view of somites, antennae, respective appendages and mouthparts were drawn under a microscope equipped with a camera lucida. The specimens were deposited at the Australian Museum, Sydney, New South Wales, Australia, and the Kitakyushu Museum of Natural History and Human History, Kitakyushu, Fukuoka, Japan. The familial classification follows Takeuchi (1993). Abbreviations used are as follows; AM, the Australian Museum; KMNH, Kitakyushu Museum of Natural History and Human History; A, antenna; ABD, abdomen; GL, gill; GN, gnathopod; LL, lower lip; MD, * Corresponding author: Ichiro Takeuchi; , takeuchi@agr.ehime-u. ac.jp mandible; MX, maxilla; MXP, maxilliped; P, pereopod; UL, upper lip; L, left; R, right. The setal formula (1-x-y-1 or 1-x-1) is used to describe the setae present on mandibular palp article 3. Family Caprellidae Leach, 1814 Genus Orthoprotella Mayer, 1903 Orthoprotella spinigera Mori, 1996 (Figs. 1 4) Orthoprotella spinigera Mori, 1996, , figs 1 5. Materials studied. 1 male, KMNH IvR 500,644, mm, Oura Bay, Okinawa Island, Japan, N, E, filamentous red algae, 18 m depth, 24 Apr 2011, coll. Ms. Chihiro Nishihira. 1 male, KMNH IvR 500,645, 1 male, KMNH IvR 500,646, and 1 male, AM- P.89063, same sampling locality and data as KMNH IvR 500,644. Type locality. Tomioka, Amakusa Islands, Kyushu, Japan, N, E. Distribution. Japanese Islands in the East China Sea, recorded so far only from Kyushu and from Oura Bay, Okinawa Island. Description. Male, KMNH IvR 500,644, body length, mm (Fig. 1). Head, 0.58 mm, pereonite 1, 0.52 mm; head and pereonite 1 fused, with slight concave area between them; head with a pair of anterodorsal round projections and lacking subtriangular lateral projection below eye; eye large,

142 I. Takeuchi & Y. Inoue Fig. 1. Orthoprotella spinigera Mori, 1996, male, 12.66 mm, KMNH IvR 500,644, Oura Bay, Okinawa Island, Japan. Fig. 2. Orthoprotella spinigera Mori, 1996, 12.

2 142 I. Takeuchi & Y. Inoue Fig. 1. Orthoprotella spinigera Mori, 1996, male, mm, KMNH IvR 500,644, Oura Bay, Okinawa Island, Japan. Fig. 2. Orthoprotella spinigera Mori, 1996, mm, KMNH IvR 500,644, Oura Bay, Okinawa Island, Japan. A, antenna; GN, gnathopod. distinctive. Pereonite 2, 2.18 mm, with a pair of anteriorly curved mid-dorsal projections, an unpaired dorsodistal projection and small anterolateral projection. Pereonite 3, 2.83 mm, longest, with a pair of mid-dorsal projections, an unpaired dorsodistal projection and round anterolateral projection. Pereonite 4, 2.71 mm, with a pair of minute mid-dorsal projections. Pereonite 5, 2.64 mm with small anterolateral projection. Pereonites 6 and 7 fused, 1.20 mm. Antenna 1, 1.25 body length; peduncular article 2 longest, 3.33 article 1; article 3, 0.9 article 2; flagellum with 14 articles, proximal article composed of 4 articles (Fig. 2 A1). Antenna 2 slender, 0.5 antenna 1; flagellum 0.15 peduncular length, with 2 articles (Fig. 2 A2). Mouthparts: Upper lip notched, wider than long, forming

3 Notes on Orthoprotella spinigera from Okinawa 143 Fig. 3. Orthoprotella spinigera Mori, 1996, mm, KMNH IvR 500,644, Oura Bay, Okinawa Island, Japan. LL, lower lip; MD, mandible; MX, maxilla; MXP, maxilliped; UL, upper lip; L, left; R, right. rounded quadrilateral projections (Fig. 3 UL). Lower lip well developed, finely setose on inner and outer lobes (Fig. 3 LL). Mandible right incisor with 5 teeth followed by lacinia mobilis with 3 teeth, 2 bundled setae and fine short setae in row; molar well developed with a molar flake, truncate; palp 3 articulate; article 2 with 6 setae; article 3 with setal formula (Fig. 3 MD (R)). Mandible left incisor with 5 teeth followed by lacinia mobilis with 5 teeth and 3 bundled setae; molar lost during dissection; article 2 with 7 setae; article 3 with setal formula (Fig. 3 MD (L)). Maxilla 1 outer plate with 7 stout apical setal-teeth; palp biarticulate; article 2 elongated with 5 stout apical setae and 7 lateral setae (Fig. 3 MX1). Maxilla 2 inner plate with 9 apical setae; outer plate with 8 apical setae (Fig. 3 MX2). Maxilliped inner plate (basal endite) subrectangular with 2 stout teeth and 3 plumose setae apically (Fig. 3 MXP); outer plate (ischial endite) 2.3 inner plate; inner margin with many blade-like setae and 2 setae medially; palp 4 articulate; article 2 longest and setose on inner margin; article 3, 1.5 article 1 with large triangular distal projection, setose on inner margin; palp article 4 (dactylus) falcate, with row of fine setae on inner margin. Pereon. Gnathopod 1 basis subequal to ischium, merus and carpus combined; carpus subtriangular, longer than wide (2 width) and setose posterodistally; propodus subtriangular, longer than wide (2.5 width) with 4 rows of lateral setae; palm begins 1/8 along posterior margin with 1 proximal seta, serriformed teeth along 2/3 of palm; dactylus slightly curved distally, inner margin with serriformed teeth (Fig. 2 GN1). Gnathopod 2 begins 1/4 along anterior margin of pereonite 2; basis 0.8 pereonite 2, scarcely setose, with an anterodistal projection; carpus triangular; propodus enlarged, subovate and subequal with basis; palm proximal projection with a robust seta (grasping spine), mid-palmar projection followed by a deep sinus and well-developed triangular projection; palm setose; dorsodistal margin of propodus strait with ca. 20 setae; dactylus falcate, with several fine setae (Fig. 2 GN2). Gill 3 elongate, 0.4 pereonite 3. Pereopod 3 slender, 0.1 pereonite 3, 1 articulate with ca. 15 distal setae and 6 small triangular plates apically (Figs. 4 P3, P3 & GL3). Gill 4 elongate, 0.35 pereonite 4. Pereopod 4 similar with pereopod 3 (Figs. 4 P4, P4 & GL4). Pereopod 5 well developed; carpus 1.3 of propodus, with ca. 15 spines along inner margin; propodus palm with a pair of proximal grasping spines; dactylus falcate (Fig. 4 P5). Pereopod 6 more robust than pereopod 5; basis subequal with carpus; propodus longest, 1.2 carpus; palm with a pair of proximal grasping spines; dactylus falcate (Fig. 4 P6). Pereopod 7 more robust than pereopod 6 (Fig. 4 P7) Pleon. Penes bilolate. 3 setae present between penes and uropod 1. Uropod 1 peduncle elongate, 2 width, with ca. 10 apical setae; ramus elongate, 3 width, with an apical seta and 2 lateral setae. Uropod 2 ramus vestigial, basal part fused with abdomen. Telson with 2 pairs of fine setae and a pair of

4 144 I. Takeuchi & Y. Inoue Fig. 4. Orthoprotella spinigera Mori, 1996, mm, KMNH IvR 500,644, Oura Bay, Okinawa Island, Japan. ABD, abdomen; GL, gill; GN, gnathopod; P, pereopod. plumose setae (Fig. 4 ABD). Remarks. Mori (1996) described Orthoprotella spinigera Mori, 1996 collected from a rope tied to a buoy at 3 m depth in Tomioka, Amakusa Islands, western Kyushu, Japan. Mori s (1996) description of the male is similar to the present description in the following: (1) antenna 1 is longer than the body length; (2) the head has a pair of anterodorsal projections; (3) pereonites 2 and 3 have a pair of anteriorly curved mid-dorsal projections and an unpaired dorsodistal projection; (4) mandibular palp article 3 has a setal fomula 1- ca or 3-1; and (5) the ramus of uropod 1 is elongated with an apical seta. The male specimens in the present study agree well with the original description of Mori (1996), except for a few minor differences, such as a body length of mm vs mm (Mori, 1996); the presence (vs. absence) of a small anterolateral projection on pereonite 2; and pereopods 3 and 4 with ca. 5 small triangular apical plates and 15 distal setae (vs. single minute apical projection with 7 setae; Mori, 1996). The present study is the second record for O. spinigera. Oura Bay, on the east coast of Okinawa Island is situated ca. 700 km south of the type locality of O. spinigera. In the marine ecoregions proposed by Spalding et al. (2007), Okinawa Island is situated in the middle of the South Kuroshio of the Central Indo-Pacific and the East China Sea of the Temperate Northern Pacific. While the Amakusa Islands are situated in the East China Sea, they include a hard coral community composed of 50 species of scleractinian corals (reported from the coastal area of Satsukigaura, Amakusa Islands; Nozawa et al. 2008). The prevalence of hard corals in the Amakusa Islands might be explained by the poleward range extension of hard corals along the coasts of the Japanese Archipelago in response to rising seawater temperatures (Yamano et al. 2011). Thus, it may be inferred that O. spinigera is widely distributed on the coasts of subtropical islands in the Japanese Archipelago. When compared to other species, the present specimens are most similar to Metaprotella sandalensis Mayer, 1898, in having: a longer antenna 1; the head with a pair of dorsal projections; pereonites 2 to 3 possessing dorsal projections; and slender pereopods 5 to 7. The fusion or distinct segmentation of pereonites 6 and 7 is an important character in the generic diagnosis of the Caprellidea (see Takeuchi & Lowry 2007, Lim & Takeuchi 2012, Takeuchi et al. 2014). The genera Metaprotella and Orthoprotella differ in one diagnosis: pereonites 6 and 7 are partially fused in Orthoprotella, while in Metaprotella pereonites 6 and 7 are completely fused. Recently, Lim & Takeuchi (2012) redescribed a male and female M. sandalensis in detail, from newly-collected material from Lifou Island, New Caledonia, the type locality. They also illustrated the distinctive characters for the species M. sandalensis Mayer, Compared with those descriptions and figures, O. spinigera differs from M. sandalensis in the following characteristics: (1) the head has a pair of apically rounded projections in O. spinigera, vs. a pair of anteriorly curved triangular projections in M. sandalensis; (2) the triangular projection below the eye absent vs. present; (3) antenna 1 is longer,

5 Notes on Orthoprotella spinigera from Okinawa 145 about 1.25 body length, vs body length; (4) article 3 of both mandibular palps has more than twice the density of fine setae, with a setal formula of 1- ca or 3-1, vs. 1-ca ; (5) the propodus of gnathopod 2 propodus of O. spinigera is more setose at the dorsodistal margin than in M. sandalensis; (6) longer pereonites 6 and 7 combined, about 0.45 pereonite 5, vs. about 0.25 pereonite 5; and (7) the uropod is elongated, with a peduncle length 2 its width, vs. short with a peduncle length less than 0.5 its width. Acknowledgements We express our sincere thanks to Mr. K. Watanabe and Ms. C. Nishihira of the diving team diving team Snack Snufkin for providing the present specimens and Ms. J.H.C. Lim for her critical reading and constructive comments on the MS. References Laubitz DR (1991) Crustacea Amphipoda Caprellidea: caprellids from the western Pacific (New Caledonia, Indonesia and the Philippines). In: Résultats des Campagnes MUSORSTOM, Volume 9 (ed Crosnier A). Mém Mus Nat Hist Nat 152: Lim JHC, Takeuchi I (2012) The distinctive species characteristics of Metaprotella sandalensis Mayer, 1898 (Crustacea: Amphipoda), commonly distributed throughout the tropical West Pacific coasts. Raffles Bull Zool 60: Mayer P (1898) Metaprotella sandalensis n.sp. In: Zoological results based on material from New Britain, New Guinea, Loyalty Island and elsewhere, collected during the years of 1895, 1896, and 1897 (ed Willey A), Cambridge, pp Mayer P (1903) Die Caprelliden der Siboga-Expedition. Siboga-Expeditie, 34: 1 160, pls McCain JC, Steinberg JE (1970) Amphipoda-1, Caprellidea-1. Crust Catalog 2: Mori A (1996) A new species of Orthoprotella (Crustacea: Amphipoda: Caprellidea) from Amakusa, Western Kyushu, Japan. Publ Seto Mar Biol Lab 37: Müller HG (1990) New species and records of coral reef inhabiting Caprellidae from Bora Bora and Moorea, Society Islands (Crustacea: Amphipoda). Revue Suisse Zool 97: Nozawa Y, Tokeshi M, Nojima S (2008) Structure and dynamics of a high-latitude scleractinian coral community in Amakusa, southwestern Japan. Mar Ecol Prog Ser 358: Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, Mc- Manus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience 57: Takeuchi, I (1993) Is the Caprellidea a monophyletic group? J Nat Hist 27: Takeuchi I, Lim JHC, Inoue Y (2014) Description of two species of Protella Dana, 1852 (Crustacea: Amphipoda); P. gracilis Dana, 1853 from Balabac Strait, the Philippines, and P. amamiensis, new species, from southern Japan. Raffles Bull Zool 62: Takeuchi I, Lowry JK (2007) Description of Metaprotella haswelliana (Mayer, 1882) (Crustacea: Amphipoda: Caprellidae) from Western Australia with designation of a neotype. Zootaxa 1466: Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Letters 38: L04601.

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