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New species and new records of pinnotherid crabs (Crustacea: Decapoda: Brachyura) from the Yellow Sea
Zoologischer Anzeiger 250 (2011) 488–496
New species and new records of pinnotherid crabs (Crustacea: Decapoda: Brachyura) from the Yellow Sea Wei Jiang, Ruiyu Liu∗ Institute of Oceanology, Chinese Academy of Sciences, 266071 Qingdao, China Received 9 May 2011; accepted 9 May 2011
Abstract Five species belonging to two genera of pinnotherid crabs are reported from the Yellow Sea. Two are new to science, namely: Sakaina glabra sp. nov. and Sakaina granulata sp. nov.; while three species are recorded for the first time from China: Pinnaxodes major Ortmann, 1894, Pinnaxodes mutuensis Sakai, 1939, and Sakaina japonica Serène, 1964. Sakaina glabra can be easily distinguished from congeners by lacking a thick rim of pubescence along the anterolateral margin of the carapace. Sakaina granulata closely resembles S. asiatica (Sakai, 1933), but differs mainly in having a row of granule-like denticles along the anterolateral margin of its carapace. © 2011 Elsevier GmbH. All rights reserved. Keywords: Crustacea; Brachyura; Pinnotheridae; Sakaina; Pinnaxodes; New species; New records; Yellow Sea
1. Introduction Species of Pinnotheridae De Haan, 1833 (sensu Ng et al., 2008; Campos, 2009; Ng and Ngo, 2010) are rarely reported from China. Shen (1932) recognized nine pinnotherid species from northern China, while Dai et al. (1980) recorded eight species from Hainan. Dai et al. (1986) recognized a total of 17 species from Chinese waters. However, no additional material from northern China has been recorded since then. While examining pinnotherid specimens collected from the Yellow Sea, the authors found five interesting species, of which two species of Sakaina Serène, 1964, are new to science, with two species of Pinnaxodes Heller, 1865, and Sakaina japonica Serène, 1964, new records for Chinese waters. The two genera, Pinnaxodes and Sakaina, are also recorded for the first time from China. This paper describes the two new species of Sakaina and presents taxonomic notes of the three new records. ∗ Corresponding
author. E-mail address: [email protected] (R. Liu).
0044-5231/$ – see front matter © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.jcz.2011.05.001
The following abbreviations are used: CL = carapace length, CW = carapace width, P2–P5 = first to fourth ambulatory legs, respectively; MXP3 = third maxilliped; G1 = male first gonopod; and G2 = male second gonopod. Measurements provided are expressed (in millimetres) as carapace length × carapace width. Specimens examined are deposited in the Marine Biological Museum, Chinese Academy of Sciences (MBMCAS) in Qingdao.
2. Systematics Family Pinnotheridae De Haan, 1833 Subfamily Pinnotherinae De Haan, 1833
2.1. Genus Pinnaxodes Heller, 1865 Pinnaxodes major Ortmann, 1894 (Fig. 1) Pinnaxodes major Ortmann, 1894: 697, pl. 23, fig. 10. – Tesch, 1918: 249 (list), 255 (key), 286 (list). – Balss, 1922: 140. – Yokoya, 1928: 778. – Sakai, 1935: 200, text-fig.
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Fig. 1. Pinnaxodes major Ortmann, 1894 (MBM 119733): (A) overall view of female (13.4 mm × 16.0 mm); (B) overall view of male (9.0 mm × 10.8 mm); (C) G1; (D) tip of G1; (E) male abdomen; (F) MXP3 (male). Scale bar indicates 1 mm (C, E, F) or 0.2 mm (D).
104; 1939: 593, text-fig. 80; 1976: 578, fig. 317a, pl. 202, figs. 4–5. – Kobjakova, 1967: 244. – Schmitt et al., 1973: 35. – Takeda and Masahito, 2000: 99, figs. 3, 4. – Ng and Manning, 2003: 915, fig. 6. – Ng et al., 2008: 250 (listed). Pinnotheres major – Sakai, 1933: 978, 980, 981, fig. 4a, b. Material examined: 1 ♂ (9.0 mm × 10.8 mm), 1 ♀ (13.4 mm × 16.0 mm) (MBM 119733), Zhucha Island, Qingdao, coll. W. Jiang, 7.01.2005. Remarks: Pinnaxodes major has been reported from Japan, Korea and the Far East of Russia. The present record extends its range further southward. The hosts of this species are variable, including the anal cavity of the sea cucumber Holothuria (Mertensiothuria) hilla Lesson, 1830 and mantle cavity of bivalves (Atrina pectinata (Linnaeus, 1767) and Mytilus sp.). Our material was found among a tray of fresh gastropod snails, Rapana venosa (Valenciennes, 1846), in a local fish market, but this may have contained other mollusks earlier, Rapana being an unlikely host. The original host is not known. Takeda and Masahito (2000) compared the two West Pacific Pinnaxodes species, P. major and P. mutuensis with the type species, P. chilensis (H. Milne Edwards, 1837), which is South American. Their conclusion was that P. major and P. chilensis are congeneric, and P. mutuensis should be removed from this genus (see below). Ng and Manning (2003: 915–917, Figs. 6, 7) pointed out the difference of MXP3
structures between P. major and P. chilensis, but continued to treat P. major as a real Pinnaxodes (see also Ng et al., 2008). More data will be needed to resolve this. Pinnaxodes mutuensis Sakai, 1939 (Fig. 2) Pinnaxodes mutuensis Sakai, 1939: 595, fig. 81a–c. – Sakai 1956: 50. – Schmitt et al., 1973: 35. – Sakai, 1976: 579, fig. 317b. – Konishi, 1977: 607, fig. 2, 3A. – Takeda and Konishi, 1991: 33, fig. 1. – Ng and Manning, 2003: 915, fig. 6E–H. Holothuriophilus mutuensis – Takeda and Masahito, 2000: 106, figs. 1B, 2G–H, 5. – Ng et al., 2008: 249 (listed). Material examined: 2 ♂♂ (6.5 mm × 6.6 mm, 3.5 mm × 4.5 mm), 2 ♀♀ (8.1 mm × 8.6 mm, 3.2 mm × 3.4 mm) (MBMCAS 119734), Haiyang Island, Dalian, N. Yellow Sea, coll. C. J. Shen, 9.15.1956. Remarks: Pinnaxodes mutuensis was reported from northern Japan by Sakai (1939, 1956, 1976) as well as Takeda and Konishi (1991) and Kornienko and Korn (2009) found the larvae in Peter the Great Bay, Russia. The present record is the first from the Yellow Sea, extending the southern limit of its distribution. The specimens were found in the mantle cavity of the bivalve Modiolus modiolus (Linnaeus). Takeda and Masahito (2000) transferred this species to the genus Holothuriophilus. Ng and Manning (2003) discussed its taxonomic status, and argued that while it was not a good species of Pinnaxodes, referring it to Holothuriophilus was
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Fig. 2. Pinnaxodes mutuensis Sakai, 1939 (MBM 119734): (A) overall view of female (8.1 mm × 8.6 mm); (B) overall view of male (6.5 mm × 6.6 mm); (C) left chela of female; (D) inside view of MXP3 (male); (E) left G1 (dorsal view); (F) tip of G1 (ventral view). Scale bar indicates 1 mm (C, D), 0.5 mm (E) or 0.1 mm (F).
also not possible because of the many marked differences between the genera. As such, they preferred to retain it in Pinnaxodes until the systematic situation is clearer. In this paper, we retain the species in Pinnaxodes for the moment (see also Ng et al., 2008).
2.2. Genus Sakaina Serène, 1964 Remarks: Schmitt et al. (1973) listed four species of Sakaina: S. asiatica (Sakai, 1933); S. incisa Sakai, 1969; S. japonica Serène, 1964, and S. yokoyai (Glassell, 1933), all from Japan. The fifth species S. koreensis Kim and Sakai, 1972, was found from South Korea (see list in Ng et al., 2008). All are small in adult size (CW no more than 1 cm or less) and mostly found amongst seaweeds. Our knowledge about the species of this genus is still limited, and it is uncertain if they are free-living or live as symbionts. The present report describes two new species of Sakaina, and records S. japonica Serène, 1964, for the first time from China. A key to the species of the genus is provided below. Key to species of Sakaina
1. CW/CL about 1.6 – CW/CL about 1.8 2. Carapace without granule-like denticles on anterolateral margins – Carapace with granule-like denticles on anterolateral margins 3. Male abdomen not incised at distal end, fingers armed with denticles – Male abdomen incised at distal end, fingers unarmed 4. CW> 5 mm, male abdomen expanded at distal end – CW< 5 mm, male abdomen not expanded at distal end 5. Tip of male abdomen almost rounded – Tip of male abdomen truncated 6. Anterolateral margins of carapace with thick rim of pubescence – Anterolateral margins of carapace without thick rim of pubescence
2 6 3 S. granulata sp. nov. 4
S. incisa 5 S. asiatica S. yokoyai S. japonica S. koreensis S. glabra sp. nov.
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Fig. 3. Sakaina glabra sp. nov., holotype female (MBM 119729): (A) overall view; (B) frontal view of carapace; (C) right cheliped; (D) abdomen; (E) P2–P5. Scale bar indicates 1 mm.
2.3. Sakaina glabra sp. nov. (Figs. 3 and 4) Material examined: Holotype ♀ (3.3 mm × 6.0 mm) (MBMCAS 119729), Yellow Sea (38◦ 20 N, 121◦ 40 E), depth 46.5 m, sandy-mud bottom, coll. M. Chen, Agassiz trawl, 7.16.1959; Paratype ♀ (3.2 mm × 5.9 mm) (MBMCAS 119730), Yellow Sea (38◦ 30 N, 121◦ 20 E), depth 54 m, fine sand and broken shells bottom, coll. J. X., Agassiz trawl, 1.28.1959. Description of holotype female: Carapace transversely oblong, 1.8 times as wide as long. Anterior and posterior portions of carapace deflexed downwards. Anterior margin weakly convex overall; posterior margin almost straight, more than half width of carapace. Front slightly
protruded beyond level of eyes, anterior edge bilobate. Eyes filling orbit; cornea pigmented, small. Dorsal surface of carapace smooth, without indication of regions except for shallow gastro-cardiac grooves, provided with a rim of pubescence behind frontal lobes forming a small triangular area, a pair of small patches of short pubescence on prebranchial region. Cardiac region slightly elevated. Chelipeds almost symmetrical; merus small, pubescent on outer surface, upper inner and abdominal edge; carpus swollen with upper inner angle slightly produced, pubescent on upper inner edge; propodus swollen, upper inner edge provided with 5 granules; fingers armed with 7 denticles on cutting edges.
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Fig. 4. Sakaina glabra sp. nov., holotype female (MBM 119729): (A) overall view; (B) left MXP3 (ventral view); (C) left MXP3 (dorsal view); (D) dorsal view of right cheliped; (E) abdomen. Scale bar indicates 1 mm (A, D, E) or 0.5 mm (B,C).
Walking legs mostly pubescent, P2 and P3 subequal in length, thickness; P4 smaller, relatively more slender. P5 conspicuously reduced. Merus of P2 triangular in cross-section, anterior surface concave; posterior surface almost flattened, lower surface slightly convex. Merus of P2 to P5 slightly depressed. Dactylus of each leg moderately curved inwards, tip sharp, dark in color. Abdomen 7-segmented including telson, widest at the third segment, behind which lateral margins of 4th to 6th segments distally convergent; tip of telson truncated; lateral margin with long pubescence. Etymology: From glaber, Latin, in reference to the smooth carapace characteristic of the species. Remarks: Sakaina glabra sp. nov. from the Yellow Sea closely resembles S. koreensis Kim and Sakai, 1972, from Impo Dolsan-do Island, South Korea. Both have relatively wider carapaces (CW/CL > 1.8) compared to congeners, but S. glabra can be easily distinguished by having a small patch of short pubescence instead of a thick rim of
pubescence along the anterolateral margin. The marginal rim of pubescence is also characteristic in other congeners. In S. glabra, the dactylus of each leg is stout and moderately curved (Fig. 4A), rather than strongly curved inwards in S. koreensis (see Kim and Sakai, 1972: Fig. 1). In addition, the female abdomen of S. glabra is relatively wider than that of S. koreensis; and the telson of S. glabra is truncated at the distal end but rounded in S. koreensis (see Kim and Sakai, 1972: Fig. 2). These differences argue for recognizing S. glabra as a separate species.
2.4. Sakaina granulata sp. nov. (Figs. 5 and 6) Material examined: Holotype ♀ (2.4 mm × 3.9 mm), (MBMCAS 119731), subtidal zone, Xinghai Park, Dalian, Liaoning Province, coll. E. F. Gurjanova, 10.24.1958. Description of holotype female: Carapace relatively small but well calcified, transversely oblong, 1.6 times as wide as
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Fig. 5. Sakaina granulata sp. nov., holotype female (MBM 119731): (A) dorsal view of carapace; (B) frontal view of carapace; (C) P2–P5; (D) antero-lateral margins (right); (E) antero-lateral margins (left); (F) inner view of left chela. Scale bar indicates 1 mm.
long, anterior and posterior portions of carapace deflexed downwards, lateral margins weakly convergent backwards; anterior margin weakly convex as a whole, posterior margin almost straight, more than half width of carapace. Front slightly protruded, anterior edge bilobate. Eyes filling orbit; cornea small, not reduced. Dorsal surface of carapace smooth, without indication of regions except for shallow gastro-cardiac grooves, with a rim of pubescences behind frontal lobes forming a small triangular area. Anterolateral margin of carapace evenly rounded, with a thin rim of pubescence, not reaching to external orbital angle, extending posteriorly towards junction of anterolateral and posterolateral margins; a row of granule-like denticles below pubescence (9 on right, 3 on left). Cardiac region slightly elevated. Chelipeds almost symmetrical, merus small, pubescent on upper inner and abdominal edges. Carpus swollen with upper inner angle slightly produced, pubescent. Propodus swollen, upper inner edge with 4 granules. Fingers with irregular denticles on cutting edges.
Walking legs mostly pubescent, first and second pair subequal in length, thickness; third pair smaller, relatively more slender. Last pair conspicuously reduced. Merus of P2 triangular in cross-section; anterior surface concave; posterior surface almost flattened, lower surface slightly convex. Merus of P2 to P5 somewhat depressed. Dactylus of each leg moderately curved inwards, tip sharp, dark in color. Abdomen 7-segmented including telson, widest at third segment, behind which lateral margins of 4th to 6th segments distally convergent; lateral margins of 6th segment nearly straight; tip of telson round; lateral margin with short pubescence. Etymology: Named granulata, Latin, in reference to the rows of granule-like denticles along the anterolateral margins of the carapace, which is diagnostic of this species. Remarks: Sakaina granulata sp. nov. is closest to S. asiatica (Sakai, 1933) from Japan. In S. granulata, the outer margin of the ischio-merus of MXP3 is straight (Fig. 6C), rather than slightly curved in S. asiatica (see Sakai, 1933: Text-fig. 3a). The distinct marginal rows of denticles on the
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Fig. 6. Sakaina granulata sp. nov., holotype female (MBM 119731): (A) dorsal view of carapace; (B) outer view of left chela; (C) right MXP3 (ventral view); (D) abdomen. Scale bar indicates 1 mm (A, B) or 0.5 mm (C, D).
dorsal carapace of S. granulata (Fig. 5D, E; Fig. 6A) also easily separate it from congeners. Compared to S. asiatica (see Sakai, 1933: Text-fig. 3, Pl. 13, Fig. 2), the cornea of S. granulata also lacks pigment but is not reduced.
2.5. Sakaina japonica Serène, 1964 (Fig. 7) Sakaina japonica Serène, 1964: 273, text-fig. 22, pl. 24, fig. B. – Sakai, 1965: 180, pl. 88, fig. 3. – Schmitt et al., 1973: 96. – Sakai, 1976: 580, fig. 319, pl. 201, fig. 2. – Sakai, 1983: 17, pl. 6 A. – Takeda et al., 1991: 92, fig. 3D–F, 4C–D. – Takeda et al., 2000: 138. – Ng et al., 2008: 251 (list).
Material examined: 1 ♂ (3.0 mm × 5.1 mm) (MBMCAS 119732), Qingdao, coll. Z. Fan and J. Xu, 11.17.1963. Remarks: The type locality of Sakaina japonica is Sagami Bay, Japan. The present record from Qingdao is the first one outside of Japan and extends its range southwards. Serène (1964) mentioned that the marginal thick rim of pubescence begins a little behind the outer end of the orbit, with 2 or 3 very small granules at the top of the curved anterolateral edges, while the rim of pubescence of our specimen begins a little further from the outer end of the orbit and the anterolateral edges remain smooth. However, the other characters are almost identical with Serène’s (1964) description and figures and we are confident they are conspecific.
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Fig. 7. Sakaina japonica Serène, 1964, male (MBM 119732): (A) overall view; (B) front view of carapace; (C) ventral view of carapace; (D) abdomen; (E) right G1 (dorsal view); (F) P2–P5. Scale bar indicates 1 mm (D, F) or 0.5 mm (E).
Acknowledgements We are thankful to Prof Yongliang Wang and Prof Xianqiu Ren for providing the information of the specimens, and to Mr. Zhao Zhang for his help during the sampling. We are furthermore grateful to Prof P. K. L. Ng for his kind advice. This project was supported by the Knowledge Innovation Program of CAS under Grant No. KZCX2-YW-417.
References Balss, H., 1922. Östasiatische Decapoden. IV. Die Brachyrhynchen (Cancridea). Archiv für Naturgeschichte 88A (11), 94–166, figs 1–2, pls 1–2. Campos, E., 2009. A new species and two new genera of pinnotherid crabs from the northeastern Pacific Ocean, with a reappraisal
of the subfamily Pinnotherinae de Haan, 1833. Zootaxa 2022, 29–44. Dai, A.Y., Feng, Z.Q., Song, Y.Z., Guo, G.X., 1980. New species and new records of family Pinnotheridae from Hainan Island. Acta Zootaxon. Sinica 5 (2), 129–143 (in Chinese with English summary). Dai, A.Y., Yang, S.L., Song, Y.Zh., Chen, G.X., 1986. Crabs of the China Seas China. Ocean Press, Beijing, 11 + 642 p. (in Chinese). Kim, H.S., Sakai, T., 1972. A new pinnotherid crab of the genus Sakaina (Decapod Crustaceans) from Korea. Proceeding of the Japanese Society of Systematic Zoology 8, 29–31. Kobjakova, Z.I., 1967. Decapoda (Crustacea Decapoda) from the Possjet Bay (the Sea of Japan). Biocoenoses of the Possjet Bay of the Sesa of Japan (Hydrobiological Investigations by Means of Aqualungs). Exploration of the Fauna of the Seas 5, 230–247, Leningrad. Konishi, K., 1977. On three species of the pinnotheid crabs from Hokkaido, Japan. Journal of the Faculty ofScience
496
W. Jiang, R. Liu / Zoologischer Anzeiger 250 (2011) 488–496
Hokkaido University, Series VI Zoology 20 (4), 605–610, pl. 21. Kornienko, E.S., Korn, O.M., 2009. Illustrated key for the identification of brachyuran zoeal stages (Crustacea: Decapoda) in the plankton of Peter the Great Bay (Sea of Japan). Journal of the Marine Biological Association of the United Kingdom 89 (2), 379–386. Ng, P.K.L., Guinot, D., Davie, P.J.F., 2008. Systema Brachyurorum. Part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bulletin of Zoology, Supplement 17, 1– 286. Ng, P.K.L., Manning, R.B., 2003. On two new genera of pea crabs parasitic in holothurians (Crustacea: Decapoda: Brachyura: Pinnotheridae) from the Indo-West Pacific, with notes on allied genera. Proceedings of the Biological Society of Washington 116 (4), 901–919. Ng, P.K.L., Ngo, V.T., 2010. Solenotheres prolixus, a new genus and new species of pinnotherid crab (Crustacea: Decapoda: Brachyura) associated with the razor clam, Solen corneus Lamarck, 1818 (Solenidae) in Vietnam. Zootaxa 2570, 61– 68. Ortmann, A., 1894. Abtheilung: Brachyura (Brachyura genuina Boas), III. Unterabtheilung: Cancroidea, 2. Section: Cancrinea, 2. Gruppe: Catometopa. Die Decapoden-Krebse des Strassburger Museums, mit besonderer Berücksichtigung der von Herrn Dr. Döderlein bei Japan und bei den Liu-KiuInseln gesammelten und zur Zeit im Strassburger Museum aufbewahrten Formen. VIII. Theil. Zoologische Jahrbücher, Abtheilung für Systematik, Geographie und Biologie der Thiere 7, 683–772, pl. 23. Sakai, T., 1933. A new genus and sorne new species of Crabs from Simoda. Science Reports of the Tokyo Bunrika Daigaku, B 12, 137–144, pl. 13. Sakai, T., 1935. Crabs of Japan, 66 Plates in Life Colours with Descriptions. Sanseido, Tokyo, x + 239 + 12 [literature cited] + 27 p [bibliography and index], 66 pls (in Japanese). Sakai, T., 1939. Studies on the Crabs of Japan IV. Brachygnatha, Brachyrhyncha. Yokendo Co., Ltd., Tokyo, pp. 365–741. Sakai, T., 1965. The Crabs of Sagami Bay Collected by His Majesty the Emperor of Japan. Maruzen, Tokyo, xvi + 206 [English
text] + 92 [Japanese text] + 32 pp [bibliography and indices], 100 pls, 1 map. Sakai, T., 1976. Crabs of Japan and the Adjacent Seas, vol. 1. Kodansha Co., Ltd., Tokyo [English text], xxix + 773 p., 379 figs, 3 maps. Sakai, T., 1983. Description of a new genera and species of Japanese crabs, together with systematically and biogeographically interesting species. Researches on Crustacea 12, 1–44, pls 1–8, 1 frontispiece. Schmitt, W.L., McCain, J.C., Davidson, E.S., 1973. Decapoda I: Brachyura I: Fam Pinnotheridae. In: Gruner, H.-E., Holthuis, L.B. (Eds.), Crustaceorum Catalogus, vol. 3., pp. 1–160. Serène, R., 1964. Goneplacidae et Pinnotheridae récoltés par le Dr. Mortensen. Papers from Dr. Th. Mortensen’s Pacific Expedition 1914–1916, part 80. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening I København 126, 181–282, pls. 16–24. Shen, C.J., 1932. The Brachyuran Crustacea of North China. Zoologica Sinica Series A 9 (I), 1–300, 171 text-figs, 10 pls, 1 rnap. Takeda, M., Masahito, P., 2000. Systematic notes on the pinnotherid crabs of the genus Pinnaxodes (Crustacea: Decapoda: Brachyura). Bulletin of the National Science Museum, Tokyo, Series A (Zoology) 26 (3), 99–112. Takeda, M., Maruyama, S., Konishi, K., 1991. Taxonomical and biogeographical notes on Sakaina yokoyai (Glassell) from northern Japan (Crustacea: Decapoda: Pinnotheridae). Bulletin of the Biogeographical Society of Japan 46 (9), 89–95. Takeda, M., Konishi, K., 1991. Pinnotherid crabs from Otsuchi Bay, Iwate Prefecture, northeastern Japan. In: Otsuchi Marine Research Centre Report 17, pp. 29–39, figs 1–2 (In Japanese). Takeda, M., Sakai, K., Shinomiya, S., Suga, H., 2000. Crabs from the Seto Inland Sea, southern Japan. Memoirs of the National Science Museum, Tokyo 33, 135–144. Tesch, J.J., 1918. The Decapoda Brachyura of the SibogaExpedition. II. Goneplacidae and Pinnotheridae. Siboga Expeditie Monographie 39, Cl, livre 84, 149–295, pls 7–18. Yokoya, Y., 1928. Report on the biological survey of Mutsu Bay. No. 10., Brachyura and crab-shaped Anomura. Science Report from the Tohoku Imperial University, Series 4 (3), 757–784, figs 1–8.
New species and new records of pinnotherid crabs (Crustacea: Decapoda: Brachyura) from the Yellow Sea Wei Jiang, Ruiyu Liu∗ Institute of Oceanology, Chinese Academy of Sciences, 266071 Qingdao, China Received 9 May 2011; accepted 9 May 2011
Abstract Five species belonging to two genera of pinnotherid crabs are reported from the Yellow Sea. Two are new to science, namely: Sakaina glabra sp. nov. and Sakaina granulata sp. nov.; while three species are recorded for the first time from China: Pinnaxodes major Ortmann, 1894, Pinnaxodes mutuensis Sakai, 1939, and Sakaina japonica Serène, 1964. Sakaina glabra can be easily distinguished from congeners by lacking a thick rim of pubescence along the anterolateral margin of the carapace. Sakaina granulata closely resembles S. asiatica (Sakai, 1933), but differs mainly in having a row of granule-like denticles along the anterolateral margin of its carapace. © 2011 Elsevier GmbH. All rights reserved. Keywords: Crustacea; Brachyura; Pinnotheridae; Sakaina; Pinnaxodes; New species; New records; Yellow Sea
1. Introduction Species of Pinnotheridae De Haan, 1833 (sensu Ng et al., 2008; Campos, 2009; Ng and Ngo, 2010) are rarely reported from China. Shen (1932) recognized nine pinnotherid species from northern China, while Dai et al. (1980) recorded eight species from Hainan. Dai et al. (1986) recognized a total of 17 species from Chinese waters. However, no additional material from northern China has been recorded since then. While examining pinnotherid specimens collected from the Yellow Sea, the authors found five interesting species, of which two species of Sakaina Serène, 1964, are new to science, with two species of Pinnaxodes Heller, 1865, and Sakaina japonica Serène, 1964, new records for Chinese waters. The two genera, Pinnaxodes and Sakaina, are also recorded for the first time from China. This paper describes the two new species of Sakaina and presents taxonomic notes of the three new records. ∗ Corresponding
author. E-mail address: [email protected] (R. Liu).
0044-5231/$ – see front matter © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.jcz.2011.05.001
The following abbreviations are used: CL = carapace length, CW = carapace width, P2–P5 = first to fourth ambulatory legs, respectively; MXP3 = third maxilliped; G1 = male first gonopod; and G2 = male second gonopod. Measurements provided are expressed (in millimetres) as carapace length × carapace width. Specimens examined are deposited in the Marine Biological Museum, Chinese Academy of Sciences (MBMCAS) in Qingdao.
2. Systematics Family Pinnotheridae De Haan, 1833 Subfamily Pinnotherinae De Haan, 1833
2.1. Genus Pinnaxodes Heller, 1865 Pinnaxodes major Ortmann, 1894 (Fig. 1) Pinnaxodes major Ortmann, 1894: 697, pl. 23, fig. 10. – Tesch, 1918: 249 (list), 255 (key), 286 (list). – Balss, 1922: 140. – Yokoya, 1928: 778. – Sakai, 1935: 200, text-fig.
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Fig. 1. Pinnaxodes major Ortmann, 1894 (MBM 119733): (A) overall view of female (13.4 mm × 16.0 mm); (B) overall view of male (9.0 mm × 10.8 mm); (C) G1; (D) tip of G1; (E) male abdomen; (F) MXP3 (male). Scale bar indicates 1 mm (C, E, F) or 0.2 mm (D).
104; 1939: 593, text-fig. 80; 1976: 578, fig. 317a, pl. 202, figs. 4–5. – Kobjakova, 1967: 244. – Schmitt et al., 1973: 35. – Takeda and Masahito, 2000: 99, figs. 3, 4. – Ng and Manning, 2003: 915, fig. 6. – Ng et al., 2008: 250 (listed). Pinnotheres major – Sakai, 1933: 978, 980, 981, fig. 4a, b. Material examined: 1 ♂ (9.0 mm × 10.8 mm), 1 ♀ (13.4 mm × 16.0 mm) (MBM 119733), Zhucha Island, Qingdao, coll. W. Jiang, 7.01.2005. Remarks: Pinnaxodes major has been reported from Japan, Korea and the Far East of Russia. The present record extends its range further southward. The hosts of this species are variable, including the anal cavity of the sea cucumber Holothuria (Mertensiothuria) hilla Lesson, 1830 and mantle cavity of bivalves (Atrina pectinata (Linnaeus, 1767) and Mytilus sp.). Our material was found among a tray of fresh gastropod snails, Rapana venosa (Valenciennes, 1846), in a local fish market, but this may have contained other mollusks earlier, Rapana being an unlikely host. The original host is not known. Takeda and Masahito (2000) compared the two West Pacific Pinnaxodes species, P. major and P. mutuensis with the type species, P. chilensis (H. Milne Edwards, 1837), which is South American. Their conclusion was that P. major and P. chilensis are congeneric, and P. mutuensis should be removed from this genus (see below). Ng and Manning (2003: 915–917, Figs. 6, 7) pointed out the difference of MXP3
structures between P. major and P. chilensis, but continued to treat P. major as a real Pinnaxodes (see also Ng et al., 2008). More data will be needed to resolve this. Pinnaxodes mutuensis Sakai, 1939 (Fig. 2) Pinnaxodes mutuensis Sakai, 1939: 595, fig. 81a–c. – Sakai 1956: 50. – Schmitt et al., 1973: 35. – Sakai, 1976: 579, fig. 317b. – Konishi, 1977: 607, fig. 2, 3A. – Takeda and Konishi, 1991: 33, fig. 1. – Ng and Manning, 2003: 915, fig. 6E–H. Holothuriophilus mutuensis – Takeda and Masahito, 2000: 106, figs. 1B, 2G–H, 5. – Ng et al., 2008: 249 (listed). Material examined: 2 ♂♂ (6.5 mm × 6.6 mm, 3.5 mm × 4.5 mm), 2 ♀♀ (8.1 mm × 8.6 mm, 3.2 mm × 3.4 mm) (MBMCAS 119734), Haiyang Island, Dalian, N. Yellow Sea, coll. C. J. Shen, 9.15.1956. Remarks: Pinnaxodes mutuensis was reported from northern Japan by Sakai (1939, 1956, 1976) as well as Takeda and Konishi (1991) and Kornienko and Korn (2009) found the larvae in Peter the Great Bay, Russia. The present record is the first from the Yellow Sea, extending the southern limit of its distribution. The specimens were found in the mantle cavity of the bivalve Modiolus modiolus (Linnaeus). Takeda and Masahito (2000) transferred this species to the genus Holothuriophilus. Ng and Manning (2003) discussed its taxonomic status, and argued that while it was not a good species of Pinnaxodes, referring it to Holothuriophilus was
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Fig. 2. Pinnaxodes mutuensis Sakai, 1939 (MBM 119734): (A) overall view of female (8.1 mm × 8.6 mm); (B) overall view of male (6.5 mm × 6.6 mm); (C) left chela of female; (D) inside view of MXP3 (male); (E) left G1 (dorsal view); (F) tip of G1 (ventral view). Scale bar indicates 1 mm (C, D), 0.5 mm (E) or 0.1 mm (F).
also not possible because of the many marked differences between the genera. As such, they preferred to retain it in Pinnaxodes until the systematic situation is clearer. In this paper, we retain the species in Pinnaxodes for the moment (see also Ng et al., 2008).
2.2. Genus Sakaina Serène, 1964 Remarks: Schmitt et al. (1973) listed four species of Sakaina: S. asiatica (Sakai, 1933); S. incisa Sakai, 1969; S. japonica Serène, 1964, and S. yokoyai (Glassell, 1933), all from Japan. The fifth species S. koreensis Kim and Sakai, 1972, was found from South Korea (see list in Ng et al., 2008). All are small in adult size (CW no more than 1 cm or less) and mostly found amongst seaweeds. Our knowledge about the species of this genus is still limited, and it is uncertain if they are free-living or live as symbionts. The present report describes two new species of Sakaina, and records S. japonica Serène, 1964, for the first time from China. A key to the species of the genus is provided below. Key to species of Sakaina
1. CW/CL about 1.6 – CW/CL about 1.8 2. Carapace without granule-like denticles on anterolateral margins – Carapace with granule-like denticles on anterolateral margins 3. Male abdomen not incised at distal end, fingers armed with denticles – Male abdomen incised at distal end, fingers unarmed 4. CW> 5 mm, male abdomen expanded at distal end – CW< 5 mm, male abdomen not expanded at distal end 5. Tip of male abdomen almost rounded – Tip of male abdomen truncated 6. Anterolateral margins of carapace with thick rim of pubescence – Anterolateral margins of carapace without thick rim of pubescence
2 6 3 S. granulata sp. nov. 4
S. incisa 5 S. asiatica S. yokoyai S. japonica S. koreensis S. glabra sp. nov.
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Fig. 3. Sakaina glabra sp. nov., holotype female (MBM 119729): (A) overall view; (B) frontal view of carapace; (C) right cheliped; (D) abdomen; (E) P2–P5. Scale bar indicates 1 mm.
2.3. Sakaina glabra sp. nov. (Figs. 3 and 4) Material examined: Holotype ♀ (3.3 mm × 6.0 mm) (MBMCAS 119729), Yellow Sea (38◦ 20 N, 121◦ 40 E), depth 46.5 m, sandy-mud bottom, coll. M. Chen, Agassiz trawl, 7.16.1959; Paratype ♀ (3.2 mm × 5.9 mm) (MBMCAS 119730), Yellow Sea (38◦ 30 N, 121◦ 20 E), depth 54 m, fine sand and broken shells bottom, coll. J. X., Agassiz trawl, 1.28.1959. Description of holotype female: Carapace transversely oblong, 1.8 times as wide as long. Anterior and posterior portions of carapace deflexed downwards. Anterior margin weakly convex overall; posterior margin almost straight, more than half width of carapace. Front slightly
protruded beyond level of eyes, anterior edge bilobate. Eyes filling orbit; cornea pigmented, small. Dorsal surface of carapace smooth, without indication of regions except for shallow gastro-cardiac grooves, provided with a rim of pubescence behind frontal lobes forming a small triangular area, a pair of small patches of short pubescence on prebranchial region. Cardiac region slightly elevated. Chelipeds almost symmetrical; merus small, pubescent on outer surface, upper inner and abdominal edge; carpus swollen with upper inner angle slightly produced, pubescent on upper inner edge; propodus swollen, upper inner edge provided with 5 granules; fingers armed with 7 denticles on cutting edges.
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Fig. 4. Sakaina glabra sp. nov., holotype female (MBM 119729): (A) overall view; (B) left MXP3 (ventral view); (C) left MXP3 (dorsal view); (D) dorsal view of right cheliped; (E) abdomen. Scale bar indicates 1 mm (A, D, E) or 0.5 mm (B,C).
Walking legs mostly pubescent, P2 and P3 subequal in length, thickness; P4 smaller, relatively more slender. P5 conspicuously reduced. Merus of P2 triangular in cross-section, anterior surface concave; posterior surface almost flattened, lower surface slightly convex. Merus of P2 to P5 slightly depressed. Dactylus of each leg moderately curved inwards, tip sharp, dark in color. Abdomen 7-segmented including telson, widest at the third segment, behind which lateral margins of 4th to 6th segments distally convergent; tip of telson truncated; lateral margin with long pubescence. Etymology: From glaber, Latin, in reference to the smooth carapace characteristic of the species. Remarks: Sakaina glabra sp. nov. from the Yellow Sea closely resembles S. koreensis Kim and Sakai, 1972, from Impo Dolsan-do Island, South Korea. Both have relatively wider carapaces (CW/CL > 1.8) compared to congeners, but S. glabra can be easily distinguished by having a small patch of short pubescence instead of a thick rim of
pubescence along the anterolateral margin. The marginal rim of pubescence is also characteristic in other congeners. In S. glabra, the dactylus of each leg is stout and moderately curved (Fig. 4A), rather than strongly curved inwards in S. koreensis (see Kim and Sakai, 1972: Fig. 1). In addition, the female abdomen of S. glabra is relatively wider than that of S. koreensis; and the telson of S. glabra is truncated at the distal end but rounded in S. koreensis (see Kim and Sakai, 1972: Fig. 2). These differences argue for recognizing S. glabra as a separate species.
2.4. Sakaina granulata sp. nov. (Figs. 5 and 6) Material examined: Holotype ♀ (2.4 mm × 3.9 mm), (MBMCAS 119731), subtidal zone, Xinghai Park, Dalian, Liaoning Province, coll. E. F. Gurjanova, 10.24.1958. Description of holotype female: Carapace relatively small but well calcified, transversely oblong, 1.6 times as wide as
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Fig. 5. Sakaina granulata sp. nov., holotype female (MBM 119731): (A) dorsal view of carapace; (B) frontal view of carapace; (C) P2–P5; (D) antero-lateral margins (right); (E) antero-lateral margins (left); (F) inner view of left chela. Scale bar indicates 1 mm.
long, anterior and posterior portions of carapace deflexed downwards, lateral margins weakly convergent backwards; anterior margin weakly convex as a whole, posterior margin almost straight, more than half width of carapace. Front slightly protruded, anterior edge bilobate. Eyes filling orbit; cornea small, not reduced. Dorsal surface of carapace smooth, without indication of regions except for shallow gastro-cardiac grooves, with a rim of pubescences behind frontal lobes forming a small triangular area. Anterolateral margin of carapace evenly rounded, with a thin rim of pubescence, not reaching to external orbital angle, extending posteriorly towards junction of anterolateral and posterolateral margins; a row of granule-like denticles below pubescence (9 on right, 3 on left). Cardiac region slightly elevated. Chelipeds almost symmetrical, merus small, pubescent on upper inner and abdominal edges. Carpus swollen with upper inner angle slightly produced, pubescent. Propodus swollen, upper inner edge with 4 granules. Fingers with irregular denticles on cutting edges.
Walking legs mostly pubescent, first and second pair subequal in length, thickness; third pair smaller, relatively more slender. Last pair conspicuously reduced. Merus of P2 triangular in cross-section; anterior surface concave; posterior surface almost flattened, lower surface slightly convex. Merus of P2 to P5 somewhat depressed. Dactylus of each leg moderately curved inwards, tip sharp, dark in color. Abdomen 7-segmented including telson, widest at third segment, behind which lateral margins of 4th to 6th segments distally convergent; lateral margins of 6th segment nearly straight; tip of telson round; lateral margin with short pubescence. Etymology: Named granulata, Latin, in reference to the rows of granule-like denticles along the anterolateral margins of the carapace, which is diagnostic of this species. Remarks: Sakaina granulata sp. nov. is closest to S. asiatica (Sakai, 1933) from Japan. In S. granulata, the outer margin of the ischio-merus of MXP3 is straight (Fig. 6C), rather than slightly curved in S. asiatica (see Sakai, 1933: Text-fig. 3a). The distinct marginal rows of denticles on the
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Fig. 6. Sakaina granulata sp. nov., holotype female (MBM 119731): (A) dorsal view of carapace; (B) outer view of left chela; (C) right MXP3 (ventral view); (D) abdomen. Scale bar indicates 1 mm (A, B) or 0.5 mm (C, D).
dorsal carapace of S. granulata (Fig. 5D, E; Fig. 6A) also easily separate it from congeners. Compared to S. asiatica (see Sakai, 1933: Text-fig. 3, Pl. 13, Fig. 2), the cornea of S. granulata also lacks pigment but is not reduced.
2.5. Sakaina japonica Serène, 1964 (Fig. 7) Sakaina japonica Serène, 1964: 273, text-fig. 22, pl. 24, fig. B. – Sakai, 1965: 180, pl. 88, fig. 3. – Schmitt et al., 1973: 96. – Sakai, 1976: 580, fig. 319, pl. 201, fig. 2. – Sakai, 1983: 17, pl. 6 A. – Takeda et al., 1991: 92, fig. 3D–F, 4C–D. – Takeda et al., 2000: 138. – Ng et al., 2008: 251 (list).
Material examined: 1 ♂ (3.0 mm × 5.1 mm) (MBMCAS 119732), Qingdao, coll. Z. Fan and J. Xu, 11.17.1963. Remarks: The type locality of Sakaina japonica is Sagami Bay, Japan. The present record from Qingdao is the first one outside of Japan and extends its range southwards. Serène (1964) mentioned that the marginal thick rim of pubescence begins a little behind the outer end of the orbit, with 2 or 3 very small granules at the top of the curved anterolateral edges, while the rim of pubescence of our specimen begins a little further from the outer end of the orbit and the anterolateral edges remain smooth. However, the other characters are almost identical with Serène’s (1964) description and figures and we are confident they are conspecific.
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Fig. 7. Sakaina japonica Serène, 1964, male (MBM 119732): (A) overall view; (B) front view of carapace; (C) ventral view of carapace; (D) abdomen; (E) right G1 (dorsal view); (F) P2–P5. Scale bar indicates 1 mm (D, F) or 0.5 mm (E).
Acknowledgements We are thankful to Prof Yongliang Wang and Prof Xianqiu Ren for providing the information of the specimens, and to Mr. Zhao Zhang for his help during the sampling. We are furthermore grateful to Prof P. K. L. Ng for his kind advice. This project was supported by the Knowledge Innovation Program of CAS under Grant No. KZCX2-YW-417.
References Balss, H., 1922. Östasiatische Decapoden. IV. Die Brachyrhynchen (Cancridea). Archiv für Naturgeschichte 88A (11), 94–166, figs 1–2, pls 1–2. Campos, E., 2009. A new species and two new genera of pinnotherid crabs from the northeastern Pacific Ocean, with a reappraisal
of the subfamily Pinnotherinae de Haan, 1833. Zootaxa 2022, 29–44. Dai, A.Y., Feng, Z.Q., Song, Y.Z., Guo, G.X., 1980. New species and new records of family Pinnotheridae from Hainan Island. Acta Zootaxon. Sinica 5 (2), 129–143 (in Chinese with English summary). Dai, A.Y., Yang, S.L., Song, Y.Zh., Chen, G.X., 1986. Crabs of the China Seas China. Ocean Press, Beijing, 11 + 642 p. (in Chinese). Kim, H.S., Sakai, T., 1972. A new pinnotherid crab of the genus Sakaina (Decapod Crustaceans) from Korea. Proceeding of the Japanese Society of Systematic Zoology 8, 29–31. Kobjakova, Z.I., 1967. Decapoda (Crustacea Decapoda) from the Possjet Bay (the Sea of Japan). Biocoenoses of the Possjet Bay of the Sesa of Japan (Hydrobiological Investigations by Means of Aqualungs). Exploration of the Fauna of the Seas 5, 230–247, Leningrad. Konishi, K., 1977. On three species of the pinnotheid crabs from Hokkaido, Japan. Journal of the Faculty ofScience
496
W. Jiang, R. Liu / Zoologischer Anzeiger 250 (2011) 488–496
Hokkaido University, Series VI Zoology 20 (4), 605–610, pl. 21. Kornienko, E.S., Korn, O.M., 2009. Illustrated key for the identification of brachyuran zoeal stages (Crustacea: Decapoda) in the plankton of Peter the Great Bay (Sea of Japan). Journal of the Marine Biological Association of the United Kingdom 89 (2), 379–386. Ng, P.K.L., Guinot, D., Davie, P.J.F., 2008. Systema Brachyurorum. Part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bulletin of Zoology, Supplement 17, 1– 286. Ng, P.K.L., Manning, R.B., 2003. On two new genera of pea crabs parasitic in holothurians (Crustacea: Decapoda: Brachyura: Pinnotheridae) from the Indo-West Pacific, with notes on allied genera. Proceedings of the Biological Society of Washington 116 (4), 901–919. Ng, P.K.L., Ngo, V.T., 2010. Solenotheres prolixus, a new genus and new species of pinnotherid crab (Crustacea: Decapoda: Brachyura) associated with the razor clam, Solen corneus Lamarck, 1818 (Solenidae) in Vietnam. Zootaxa 2570, 61– 68. Ortmann, A., 1894. Abtheilung: Brachyura (Brachyura genuina Boas), III. Unterabtheilung: Cancroidea, 2. Section: Cancrinea, 2. Gruppe: Catometopa. Die Decapoden-Krebse des Strassburger Museums, mit besonderer Berücksichtigung der von Herrn Dr. Döderlein bei Japan und bei den Liu-KiuInseln gesammelten und zur Zeit im Strassburger Museum aufbewahrten Formen. VIII. Theil. Zoologische Jahrbücher, Abtheilung für Systematik, Geographie und Biologie der Thiere 7, 683–772, pl. 23. Sakai, T., 1933. A new genus and sorne new species of Crabs from Simoda. Science Reports of the Tokyo Bunrika Daigaku, B 12, 137–144, pl. 13. Sakai, T., 1935. Crabs of Japan, 66 Plates in Life Colours with Descriptions. Sanseido, Tokyo, x + 239 + 12 [literature cited] + 27 p [bibliography and index], 66 pls (in Japanese). Sakai, T., 1939. Studies on the Crabs of Japan IV. Brachygnatha, Brachyrhyncha. Yokendo Co., Ltd., Tokyo, pp. 365–741. Sakai, T., 1965. The Crabs of Sagami Bay Collected by His Majesty the Emperor of Japan. Maruzen, Tokyo, xvi + 206 [English
text] + 92 [Japanese text] + 32 pp [bibliography and indices], 100 pls, 1 map. Sakai, T., 1976. Crabs of Japan and the Adjacent Seas, vol. 1. Kodansha Co., Ltd., Tokyo [English text], xxix + 773 p., 379 figs, 3 maps. Sakai, T., 1983. Description of a new genera and species of Japanese crabs, together with systematically and biogeographically interesting species. Researches on Crustacea 12, 1–44, pls 1–8, 1 frontispiece. Schmitt, W.L., McCain, J.C., Davidson, E.S., 1973. Decapoda I: Brachyura I: Fam Pinnotheridae. In: Gruner, H.-E., Holthuis, L.B. (Eds.), Crustaceorum Catalogus, vol. 3., pp. 1–160. Serène, R., 1964. Goneplacidae et Pinnotheridae récoltés par le Dr. Mortensen. Papers from Dr. Th. Mortensen’s Pacific Expedition 1914–1916, part 80. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening I København 126, 181–282, pls. 16–24. Shen, C.J., 1932. The Brachyuran Crustacea of North China. Zoologica Sinica Series A 9 (I), 1–300, 171 text-figs, 10 pls, 1 rnap. Takeda, M., Masahito, P., 2000. Systematic notes on the pinnotherid crabs of the genus Pinnaxodes (Crustacea: Decapoda: Brachyura). Bulletin of the National Science Museum, Tokyo, Series A (Zoology) 26 (3), 99–112. Takeda, M., Maruyama, S., Konishi, K., 1991. Taxonomical and biogeographical notes on Sakaina yokoyai (Glassell) from northern Japan (Crustacea: Decapoda: Pinnotheridae). Bulletin of the Biogeographical Society of Japan 46 (9), 89–95. Takeda, M., Konishi, K., 1991. Pinnotherid crabs from Otsuchi Bay, Iwate Prefecture, northeastern Japan. In: Otsuchi Marine Research Centre Report 17, pp. 29–39, figs 1–2 (In Japanese). Takeda, M., Sakai, K., Shinomiya, S., Suga, H., 2000. Crabs from the Seto Inland Sea, southern Japan. Memoirs of the National Science Museum, Tokyo 33, 135–144. Tesch, J.J., 1918. The Decapoda Brachyura of the SibogaExpedition. II. Goneplacidae and Pinnotheridae. Siboga Expeditie Monographie 39, Cl, livre 84, 149–295, pls 7–18. Yokoya, Y., 1928. Report on the biological survey of Mutsu Bay. No. 10., Brachyura and crab-shaped Anomura. Science Report from the Tohoku Imperial University, Series 4 (3), 757–784, figs 1–8.