Octopus sinensis d'Orbigny 1841

Octopus sinensis d’Orbigny, 1841

[English vernacular name: The East Asian common octopus] [Japanese name: Madako] (Figs 1–6, 8–11; Tables 1–2)

Octopus sinensis d’Orbigny, 1841 (text): 68; d’Orbigny 1834 (atlas of plates): pl. 9 (lower figure, without species identification: subsequently identified by Sasaki 1929: 37).

Octopus vulgaris (non Cuvier, 1797): Appellöf 1886: 7; Ortmann 1888: 642; Robson 1929: 57 (in part); Nesis 1987: 312 (in part; northwestern Pacific population); Okutani et al. 1987: 157, fig. 60 A–C; Kaneko et al. 2011: 106; Kubodera 2013: 212.

Polypus vulgaris: Wülker 1910: 5; Berry 1912: 386; Sasaki 1929: 35 (in part), text figs 11–12, pl. IV fig. 1, pl. IX figs 1–3, pl. XXIX fig. 1. (Polypus is a suppressed name; ICZN 1954).

Octopus cf. vulgaris (cf. O. sinensis): Gleadall and Salcedo- Vargas 2004: 119 (in part).

Material examined. Neotype, here designated, mature male (ML 97 mm), Ariake Sea, Hato-no-kama Harbour, Oyano Is., Kami-amakusa City, Kumamoto Pref., Kyushu, Japan, IGG 312, NSMT Mo 85659, 25.x.2013, M. Abe, I.G. Gleadall, K. Matsubara and S. Morii.

Other material examined: 1 mature male (ML 95 mm), loc. not stated (? Kyushu, Japan), NRML 2438, undated (?1824–1827), P.F. von Siebold; 1 immature female (ML 89 mm), loc. not stated (? Kyushu, Japan), NRML 472, undated (?1824–1827), P.F. von Siebold; 1 submature male (ML 107 mm), Kagoshima, Kyushu, Japan, ZUMT 994. CO-38 [056], August 1903, donated by Kagoshima Prefectural Government; 1 male ML 106 mm (head dissected, arms missing), 1 submature female ML 119 mm (no collection data), ZUMT 994.CO-20 [058]; 1 submature female (ML 84 mm), 1 juv. (ML 35 mm), Japan Sea, off Konoura, Yuri-gun, southern Akita Pref., Honshu, Japan, NSMT Mo 75758 (SHC), 17 October 1931; 1 male (ML 96 mm), Onahama, Iwaki-gun, Fukushima Pref., Honshu, Japan, NSMT Mo 75750 (SHC), January 1932; 2 males (ML 82, 68 mm), Pacific Ocean, Sendai Bay, off Yuriage, Natori-gun, Miyagi Pref., Honshu, Japan, NSMT Mo 75759 (SHC), January 1933; 1 immature male (ML 42 mm), Pacific Ocean, off Hayama, Sagami (Kanagawa Pref.), Honshu, Japan, SMI 051, 8 June 1957; 1 male (ML 56 mm), Japan Sea, Fukaura, Nishitsugaru-gun, Aomori Pref., Honshu, Japan, NSMT Mo 75739 (SHC), August 1963; 1 male (ML 72 mm), Japan Sea, Kamo Aquarium (originally caught by octopus pot), Yamagata Pref., Honshu, Japan, BMNH 1994108, Sept. 1987, I.G. Gleadall; 1 mature female (ML 122 mm), Japan Sea, Toyama Bay, Uozu, (octopus pot), Toyama Pref., Honshu, Japan, IGG 036, NSMT Mo 85656, August 1992, O. Inamura; 1 mature male (ML 93 mm), Shiriyazaki, Pacific coast of Aomori, IGG 039, NSMT Mo 85657, 22 March 1993, I.G. Gleadall and K. Noro (né Sato); 1 maturing female (ML 124 mm), East China Sea, 31°40.95′ N, 127°47.09′ E, NSMT Mo 74775, 19 June 2000, H. Horikawa, Kumamoto Maru; 1 mature male (ML 73 mm), Iyo-nada, Seto Inland Sea, Mori, Japan, in a cage, IGG 169, NSMT Mo 85658, 21 June 2003, H. Sakaguchi; 1 submature male (ML 86 mm, arm L2 with bifurcated tip), Japan Sea, Kamo, Yamagata Pref., Japan, from beach with rod and line, IGG 290 (donated to M. Amor), 22 October 2011, Y. Hino and T. Itō; 1 mature male (ML 82 mm), collected with neotype, IGG 302, NSMT Mo 85659; 2 mature males (ML 82–111) mm, collected with neotype, IGG lots 307 and 309 (donated to M. Amor); 7 mature males (ML 111–168 mm, 902– 2432 g; IGG 318, 324–328, 330), 5 submature females (ML 130–162 mm, 1542-2221 g, IGG 319–321, 323, 329), and 1 immature female (ML 112 mm, 956 g, IGG 322), Pacific Ocean, Oura Port, near Onagawa, Oshika District, Miyagi Prefecture, Honshu, Japan, landed from baited cage traps at 50–100 m [mixed catch with Enteroctopus dofleini (Wülker, 1910) of similar size], NSMT Mo 85660, 30 January 2014, F. Abe, I.G. Gleadall, K. Matsubara, and S. Morii.

Molecular sequences. NSMT Mo 74775, GenBank Accession nos. AB430548 (CO1) and AB573218 (CO3), registered (as Octopus vulgaris) by Kaneko et al. (2011).

Diagnosis. Member of the Octopus vulgaris species complex inhabiting the western North Pacific in the vicinity of Japan. Maximum size around 3 kg, males maturing around ML 70 mm (approx. 400 g), females 110 mm (approx. 900 g). Funnel organ broad, W-shaped. Ocelli absent. Mature males with 1 or 2 enlarged suckers between #12 and #15 (commonly #13 and/or #14) on arms 2 and 3; length of hectocotylized arm around 80% of length of third leπ arm, with 119–152 suckers, ending with a minute ligula (length about 3 mm). Spermatophores small, approximately 60 (each 40 mm in length) in a male of ML 92 mm. Females lay many small eggs together as a number of branched strings (festoons). Eggs hatch into planktonic paralarvae with a ML of 1.5–2.0 mm and arms each bearing 3 suckers. Well-developed ink sac and anal cirri present.

Description. Based on 23 males (14 mature, 2 submature, 1 immature, 6 maturity not assessed), 11 females (2 mature, 7 submature, 2 immature), and 1 juvenile. Medium- to large-sized octopus: maximum size around 3 kg, males maturing around ML 70 mm (approx. 400 g), females 110 mm (approx. 900 g). Body robust, ovoid (MW approx. two-thirds of ML); head broad, width just less than half of ML; neck broad, almost as wide as head (Figs 1–3). Eyes large though not especially prominent, each with a single papilla of modest size posterodorsally, a smaller one sometimes visible anterodorsally (Fig. 3).

Abbreviations: AF, arm formula (arm numbers arranged in length order, longest to shortest); AL, arm length (length of each arm pair, leπ/right); CL, calamus length; FL, funnel length; FFL, free funnel length; GC, gill count (number of gill lamellae per demibranch); GL, gill length; HW, head width; L1, L2,..., leπ arm 1, 2, etc.; LL, ligula length; MW, mantle width; NW, neck width; R1, R2,..., right arm 1, 2, etc.; Rg, regenerating arm; SC (L3/R3), sucker count (no. of suckers on 3rd arm of leπ/right side); SD, diameter of largest sucker (especially enlarged in males); SD (arms), arms with the largest suckers (particularly enlarged in males); SD (#), number of largest sucker counting distally from mouth (where more than one arm bears enlarged suckers, each value corresponds to respective SD arm); T, truncated arm; VML, ventral mantle length; WD, depth of interbrachial membrane (A–E, sectors of interbrachial membrane from dorsal to ventral); WDF, web depth formula (interbrachial membrane depths arranged in depth order, deepest to shallowest). * Originally 162mm (shrinkage detected). ** Arm R3 of this specimen has regenerated from an earlier truncation distal to sucker #43; value given is from the next longest arm, L2.

Skin with well-defined topology of raised ‘patches’ delineated by a system of recessed ‘grooves’ (Fig. 2), these not retained in specimens preserved following a delay between death and fixation (e.g., storage on ice). Primary skin colour cream-grey, typically speckled with darker shades, chromatophore expansion creating deep brick-red to brown colours when undisturbed but alert, and also when fixed (Figs 2–3). Ventral mantle smoother and paler in colour (Figs 1, 3); sucker acetabula white to grey against an oral arm surface of dark red (Fig. 4). Large skin papillae may be observed on the dorsal mantle, including 4 papillae arranged in a diamond configuration (two in the midline, and a lateral papilla on each side forming a symmetrically placed pair). Hints seen of a pair of frontal white spots on the bases of arms 1 (no other conspicuous white spots observed).

Values are either mean (±standard error) or range (min.–max.). For O. sinensis, values are from all male specimens in Table 1; and for O. vulgaris include the male specimens listed as comparative material, and data tabulated by Guerra et al. (2010); 1, data for heavily damaged specimens omitted. Abbreviations as in Table 1: suffix ‘I’ indicates an index of measurement expressed as % ML, except for CLI (CL expressed as % LL), FFLI (FFL expressed as % FL), LLI (LL expressed % length of arm R3) and OAI (opposite arm index: length of arm R3 as % of that of arm L3). SC (N) range, sucker count range for normal arms (taking the largest value for each specimen); SC (R3) range, range of number of suckers on hectocotylus (males only, for all males inspected).

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Arms long, longest around 4 times ML, shortest 3 to 3.5 times ML (growing allometrically throughout life, relatively longer in larger animals). Arms 2 and 3 subequal in length, longer than subequal arms 1 and 4, which are about 1 ML shorter than arms 2 and 3 (Fig. 2). Arm formula most commonly 2.3.4.1 (Table 1). Arms robust and muscular, broader than mantle when placed together (Figs 1–2); width of each arm approximately 15% of ML at broadest extent (which corresponds approximately to deepest extent of interbrachial membrane; Figs 1, 2, 4), narrowing gradually until distal third, then more abruptly to slender tips (Figs 1–2). Autotomy absent. Males with right arm 3 hectocotylized, shorter than opposite arm by around 20% (OAI around 80%; Table 2; cf. Fig. 2). Ligula of copulatory organ minute (Figs 5–6; LLI 1.7, Table 2; cf. Sasaki 1929, pl. IX fig. 1), closely resembling that of O. vulgaris (Fig. 7), with a relatively broad fleshy protuberance on anterior side closing ligula base (Fig. 6, Pr.; cf. Fig. 7); calamus length around 40% of that of ligula (Fig. 5; CLI 42%, Table 2), rounded, somewhat inconspicuous, not raised from surface of ligula, and with closed median groove (Fig. 6, Cal.). Spermatophore guide with pale internal surface, present as a well-defined muscular edge along the marginal membrane of R3 (Fig. 2, H; Fig. 5, SGr).

Arms bearing up to 276 suckers per normal arm in mature individuals (Tables 1–2); hectocotylized arm of males with 119–152 suckers (Table 2). Suckers robust, broad, 1 or 2 conspicuously enlarged in males between #12 and #15 (commonly #13 and/or #14) on arms 2 and 3 (cf. Fig. 4); infundibulum shallow, flared, with well-defined, scalloped rim and about 32 well-developed cushions, coalescing to around 20 centrally; acetabulum moderately deep with small opening (Fig. 4).

Interbrachial membranes (arm webs) substantial but shallow between all arms, deepest (sectors B, C and D) 80–90% of ML (WDI max, Table 2), shallowest (sectors A and E) 45– 50% of ML (WDI min, Table 2; Figs 1, 2 and 4); web depth formula typically C.D.B.E.A (Table 1).

Funnel robust, modest in length, up to 40% of ML (FLI, Table 2; Figs 1, 3), moderately narrow, tapering abruptly (Fig. 1), free for about two-thirds of its length (FFLI, Table 2; Figs 1, 3); median basal notch approximately 12% of FL. Funnel attachment is directly beneath posterior region of head, with free funnel extending just to anterior margin of eyes, well short of interbrachial membrane (Figs 1, 3). Funnel organ ‘W’ shaped, robust, with broad limbs, lateral limbs 20–25% shorter than median, occupying about half funnel length, positioned close to funnel tip.

Mantle robust, muscular, with moderately thick wall; opening wide (up to 25% wider than neck width; mantle edge length approximately 2.5 times direct width across mantle aperture; cf. Fig. 1). A pair of non-calcareous stylets present embedded in dorsolateral mantle musculature, supporting origin of funnel retractor muscle of each side; stylet length approximately half of ML, anterior section just over a quarter of total stylet length. Gills typically with 8 or 9 (range 7–10) lamellae per demibranch; relatively long (GLI 30–45; Table 2). Ink sac and anal cirri well-developed.

Spermatophores small, length around half of ML (approximately 40 mm long in a male of ML 92 mm); released from a pseudophallus of modest size (length approximately 12% of ML) with spermatophore duct entering posteriorly close to dorsomedial bulbous expansion (occupying approximately 30% of total pseudophallus length; cf. Sasaki 1929, pl. IX fig. 2a, b). Females lay small eggs in festoons made by entwining egg stalks and cementing them to hang down from roof of den. Eggs hatch into planktonic paralarvae of ML 1.5–2.0 mm and 3 suckers per arm (personal observations from aquaculture experiments).

Distribution. Known to occur in Japan as far north as southern Hokkaido and in the East China Sea off Japan (Sasaki 1929; Kaneko et al. 2011) and Taiwan (cf. Sasaki 1929; Lü et al. 2013; Reid and Wilson, 2015), although the extent of its range southwards beyond Taiwan is currently uncertain and requires further research.

Remarks. The species was named sinensis (Latin, meaning “from China ”) even though the specimens upon which d’Orbigny’s description was based are known to have come from Japan (see further discussion below). d’Orbigny himself mentioned Japan several times during the description and discussion, quoting from an original pre-Linnean Japanese text clearly identified subsequently by Sasaki (1929). The confusion with China appears to have arisen from the use of Parisian scholars of Chinese hired by d’Orbigny (1839–1848) to translate the original text, which was written in Chinese style characters (Takigawa, pers. comm.).

The date of publication of the original description (d’Orbigny 1841) was elucidated by Tillier and Boucher- Rodoni (1994), who determined that the livraison containing O. sinensis was published between 1839 and 1841. The earliest confirmed year for the publication of this description is therefore 1841 (ICZN 1999: Article 21.6; Gleadall and Salcedo-Vargas 2004). The original description by d’Orbigny was inadequate and devoid of type or locality designations but any confusion was resolved by Sasaki (1929), who provided a thorough redescription with clarification of d’Orbigny’s ambiguities including confirmation that the species in question was described from Japanese specimens (despite the specific name alluding to China).

There are no extant type specimens but it is deduced (ICZN 1999: Article 73.1.4) that the holotype is that illustrated by d’Orbigny in his atlas of plates (d’Orbigny 1834– 1842; dated 1834 by Tillier and Boucher-Rodoni 1994), Plate 9 (lower figure, without species identification; subsequently identified by Sasaki 1929). The actual specimen (holotype by illustration) has never been identified. In view of the confusion over the number of species in the Octopus vulgaris complex, and the lack of extant type material for O. sinensis, a neotype is here designated to stabilize this species name. The vouchers for O. sinensis listed above provide a range of material for reference in museums in Australia, The Netherlands, the UK and Japan for future comparisons with other closely related species of the O. vulgaris complex.

It is noted that the collection of Japanese octopus specimens by Philipp Franz von Siebold and their deposition in Leiden was probably communicated to d’Orbigny by De Haan, and that descriptions in Japanese were also present in the extensive libraries of Japanese works taken from Japan to Leiden (by von Siebold) and to Paris (d’Orbigny 1841; Sasaki 1929; Gleadall and Goud 1993; Takigawa pers. comm.). Attempts have been made to locate correspondence among the early nineteenth century scientists concerning specimens of Japanese Cephalopoda but none has been found (extensive enquiries of staff at BMNH, NRML, the National Museum of Natural History, Paris, and the Natural History Museum of La Rochelle). Japanese octopus specimens deposited in Leiden by von Siebold have been identified in the present study as O. sinensis (see list of material examined, above), corresponding to the species described by d’Orbigny (1841) as the common octopus of Japan and subsequently redescribed by Sasaki (1929).

Sasaki (1929) included Taiwan in his list of localities for O. sinensis but the exact distribution of this species in Chinese waters requires further research. The presence of O. sinensis in Taiwanese waters is confirmed from identical gene sequences obtained recently from specimens collected off Japan and Taiwan (compare for example sequences from specimens identified as O. vulgaris in the studies of Kaneko et al. 2011 and Lü et al. 2013). Sequences of the CO1 gene obtained from molecular analysis of tissue from the Japanese specimens listed here (Nishitani and Gleadall, unpublished data) were all identical to those reported elsewhere for specimens of the O. vulgaris complex from localities off East Asia (cf. Guerra et al. 2010; Kaneko et al. 2011; Amor et al. 2014). These will be submitted to a gene sequence database subsequently under the species name O. sinensis.

There is evidence of other closely related O. vulgaris -like species in East Asian waters (Gleadall unpublished; Reid and Wilson 2015) but this requires further research. The species described here as O. sinensis relates particularly to the main islands of Japan where it is a well-known, popular and sought-aπer seafood item fetching a high market value. Surveys of other localities around Japan have not detected the presence of any other species that could be confused with O. sinensis. With the description and sequences provided by the present study, which includes specimens also identified as the Japanese common octopus by Sasaki (1929), O. sinensis is now a clearly described species with which other closely related species can be compared.