Vignadula atrata, (LISCHKE, 1871)

Tan, Koh Siang, Tan, Samuel Hui Ming, Sanpanich, Kitithorn, Duangdee, Teerapong & Ambarwati, Reni, 2022, Xenostrobus or Vignadula (Bivalvia: Mytilidae)? A taxonomic re-evaluation of small black mussels inhabiting the upper intertidal zone of the estuaries of Southeast Asia, Zoological Journal of the Linnean Society 196, pp. 316-345 : 323-325

VIGNADULA ATRATA (LISCHKE, 1871)

( FIGS 1–3 , 8 , 11 , 12A , 13 )

Mytilus atratus Lischke, 1871a: 44 and Lischke, 1871b: 146, pl. 10, figs 4, 4a, 5, 5b; type locality: Nagasaki, Japan. Holotype: ZIN 2/111 (see Lutaenko & Chaban, 2016).

Modiola aterrima – Dall, 1871: 154 and pl. 14, fig. 13; type locality: Bay of Yeddo (Tokyo Bay ). Holotype: USNM 185505.

Volsella atrata – Kuroda, 1932: 134, sp. 407.

Adula atrata – Habe & Kosuge, 1967: 127, pl. 47 fig. 10.

Xenostrobus atratus – Wilson, 1967: 284; – Ockelmann, 1983: 109–110, fig. 44 (graph); – Bernard et al., 1993: 33–34 (in part); – Kimura, 1996: 97–100, figs 1–6; – Lutaenko et al., 2019: 185 and pl. 9, figs I, J.

Hormomya atrata – Habe, 1968: 167–168, pl. 50, fig. 19.

Vignadula atrata – Kuroda et al., 1971: 549 [in Japanese], 348 [in English], pl. 74, figs 5, 6; – Wang et al., 2011: 87–88, figs. 3-71.

Xenostrobus atrata – Wang, 1997: 207–208, fig. 87; – Wang, 2004: p. 229, pl. 121E.

Diagnosis: Dark purplish blue to black mytiliform shells with terminal umbones; anterior half of ventral region often yellow to orange crossed by dark purple commarginal lines; animal without plicate gland; labial palps short, each palp bearing with ≤ 16 folds; mantle edge at posterior region of animal bears up to ten simple and/or branched guard papillae.

Material examined: Japan: Fukuoka-Amakusa (NSMT 49028); Kagoshima - Shoujigawa

(ZRC.MOL.24027, 24916, 24917; PMBC 25330); Red Cross Hospital, Hirakawa (ZRC.MOL.24918, 24919); Ibusuki (ZRC.MOL.24920); Mie –Tsu (NSMT 58821); Miyagi-Fukuura Island (NSMT 44150); Nagasaki-Obama (ZRC.MOL.24921); Toishi-ko (ZRC. MOL.24922); Isomichimachi (ZRC.MOL.24923,

24924); Okayama-Kasaoka Bay (NSMT 49029). See also the Supporting Information ( Table S1 ).

Shell: Variable in outline and shape, length ≤ 15 mm, mostly entirely dark purplish blue to black over the posterior two-thirds of length of valves, while the anterior region is translucent yellow to orange crossed by fine dark purple commarginal lines where the periostracum is intact. Umbones terminal or in line with the edge of the anteroventral margin. Periostracal surface with fine, close-set commarginal lines free of byssal secretions. Ligament robust, long, stretching posteriorly from umbones to nearly half the length of the shell. Resilial pits are absent. At the region immediately below the umbones, there is a short, narrow shelf, but there are no hinge teeth anterior or posterior to the umbones. Likewise, there are no teeth posterior to the ligament. Interior of shell can generally be divided into a dark purplish brown dorsoposterior region and a lighter-coloured anteroventral region. Anterior region with prominent, oval anterior adductor muscle scar. Posterior adductor muscle scar continuous with byssal retractor muscle scars.

Shell microstructure: Shell generally comprises of two recognizable layers below the periostracum: a thin prismatic layer, under which a thick sheet nacreous layer is present. A thin, fibrous prismatic myostracum may be present within the sheet nacreous layer.

Anatomy: Inner mantle lobes forming the inhalant aperture are translucent orange-brown, with a high density of yellow subcutaneous pigment grains. The guard papillae are six to ten in number on each side. Each papilla is translucent white with small, white subcutaneous pigment grains. They may be simple or mixed with bi- or trifid papillae ( Figs 8 , 12A ). The papillae all taper to a point when fully extended. They are highly contractile and if disturbed can be withdrawn completely to appear as folds or creases along the mantle edge. Juveniles <2 mm SL do not possess guard papillae ( Fig. 8A ). Plicate organ is absent. Foot is yellowish white.

Two bundles of the posterior adductor muscle can (barely) be distinguished, and one is generally larger than the other, although their relative size varies between individuals. The posterior byssal retractor muscles are divided into two main bundles near the base of the foot. Of these, the anterior bundle is further divided into two or three bundles proximal to the shell. The pericardial complex is situated anterior to the posterior byssal retractor muscles (Category 2 of Morton, 2015a).

Labial palps vary in length according to shell size (see Theisen, 1982; Ockelmann, 1983), as does the number of folds (sorting ridges), which can range between five and 16 on each palp for SLs 4–12.5 mm (see Fig. 11 ).

Geographical distribution ( Fig. 13 ): Korea (Jeju Island; see Lutaenko et al., 2019), Japan and northeast China.

Taxonomic remarks: Mytilus atratus was first described from Nagasaki Bay, Japan by C. E. Lischke in 1871 (see Lutaenko & Chaban, 2016). Subsequent Japanese workers were undecided on its generic status, assigning the species variously to Adula H.Adams &A.Adams, 1857 , Hormomya Mörch, 1853 and Volsella Scopoli, 1777 (see Kuroda, 1932; Habe & Kosuge, 1967; Habe, 1968). A century later, the species was assigned to Vignadula Kuroda & Habe in Kuroda et al. (1971) , although Wilson (1967) recognized the possible connection between V. atratus and the Australian species of Xenostrobus . This was later followed up by Ockelmann (1983) and Lee & Morton (1985), who considered Vignadula a junior synonym of Xenostrobus . At about the same time, Limnoperna fortunei kikuchii Habe (1981) was described, which afterwards proved to be X. securis introduced from Australia and/or New Zealand ( Kimura et al., 1999). Kimura (1996) also described X. atratus in detail, and subsequently, Kimura et al. (1999) compared it with other congeners (see also Table 1 ). However, owing to its external resemblance to the tropical V. mangle (see below), the two species have sometimes been confused with each other (e.g. Wang, 1997; Liu et al., 2011), particularly along the Chinese coast, where both species may occur and overlap in distribution.

Figures

Figure 1. Concatenated four-gene Bayesian inference/maximum likelihood tree based on COI, ITS1, 28S D1R and H3 sequences of Xenostrobus mussels from East Asia and Australasia. Both 313 bp and full-length COI barcodes were used in the analysis. In several cases (e.g. SG X18 and SG X18-2; XTSW1 and XTSW1-2), two sequences from the same individual were incorporated into the analysis. For readability, some nodes on the branch tips have been omitted and the lengths of some branches truncated (marked by a double slash). Sequence codes with asterisks were obtained from specimens shown in Figures 4–7. Line and text colours correspond to the colour scheme used to differentiate the geographical distributions of the species represented in the clades A, B, C and D. Sequence code abbreviations: E Th, Gulf of Thailand; FJP, Fukuoka, Japan; GB, GenBank; HK, Hong Kong; Indon, Indonesia; J MY, Johor, Malaysia; JP, Japan; K EMY, Kuching, East Malaysia; K JP, Kagoshima, Japan; K TW, Kinmen, Taiwan; N JP, Nagasaki, Japan; P MY, Perak, Malaysia; SG, Singapore; S Indon, Surabaya, Indonesia; SW Th, south-west Thailand; Th, Thailand; Z Tan, Zanzibar, Tanzania.

Figure 2. Concatenated three-gene Bayesian inference/maximum likelihood tree based on COI, 28S D1R and H3 sequences of mussels from East Asia and Australasia, including additional sequences from GenBank. For readability, some nodes on the branch tips have been omitted and the lengths of some branches truncated (marked by a double slash). Sequence codes with asterisks were obtained from specimens shown in Figures 4–7. Line and text colours correspond to the colour scheme used to differentiate the geographical distributions of the species represented in the clades A, B, C and D.For an explanation of sequence code abbreviations, see legend to Figure 1.

Figure 3. Concatenated two-gene Bayesian inference/maximum likelihood tree based on COI and H3 sequences of mussels. For readability, some nodes on the branch tips have been omitted and the lengths of some branches truncated (marked by a double slash). Sequence codes with asterisks were obtained from specimens shown in Figures 4–7. Line and text colours correspond to the colour scheme used to differentiate the geographical distributions of the species represented in the clades A, B, C and D. For an explanation of sequence code abbreviations, see legend to Figure 1.

Figure 8. Vignadula atrata (Lischke, 1871). A, posterior region of living juvenile with extended mantle margins (imm) devoid of guard papillae. Blue and green arrows depict the direction of inhalant and exhalant currents. Scale bar: 500 µm. B, posterior region of ethanol-preserved sequenced individual XNJ 0519B, with left valve removed to show posterior end of ctenidium (ct), mixture of simple (marked by yellow crosses) and branched (yellow asterisks) guard papillae (gp) along the inner mantle margin (imm) and posterior adductor muscle (pam). Scale bar: 1 mm. C, living individual with numerous simple and branched guard papillae. Scale bar: ~500 µm. D, living individual with mostly simple guard papillae. Note the well-formed exhalant siphon. Scale bar: ~1 mm. A, Kagoshima, Japan. B–D, Nagasaki, Japan.

Figure 11. Relationship between shell size and number of folds observed on the labial palps of four Vignadula species from East and Southeast Asia. Data from Ockelmann (1983) for Vignadula atrata, Vignadula balani and Vignadula mangle are indicated separately. Apart from data points based on the study by Ockelmann (1983) and three individuals of Vignadula kuraburiensis sp. nov., all are referable to genetically sequenced individuals based on this study.

Figure 12. Guard papillae of Vignadula (A–D) and Xenostrobus (E–G) species on the posterior region of the inner mantle margin attached to LV. All animals shown preserved in ethanol. A, Vignadula atrata, SL = 11.4 mm, Toishi-ko, Nagasaki, Japan. B, Vignadula mangle comb. nov., SL = 13.5 mm, Kampong Bako, Kuching, Sarawak. C, Vignadula kuraburiensis sp. nov., SL = 13.2 mm, Kuraburi, Phangnga, Thailand. D, V. kuraburiensis sp. nov., SL = 8.8 mm, Ban Baen, Ranong, Thailand. E, Xenostrobus inconstans, SL = 22.7 mm, Dunnalley Bay, Tasmania, Australia (TMAG E21829). F, Xenostrobus securis, SL = 24.8 mm, Swan River, Perth, WA,Australia. G, Xenostrobus pulex, SL = 13.1 mm, Cottesloe, Perth, WA, Australia. Scale bars: 1 mm in A–C, E–G; 500 µm in D.

Figure 13. Geographical distribution of Vignadula and Xenostrobus species in East Asia, Australia and New Zealand. Locations are based on examined museum material or material collected in the field for this study by the authors, and supplemented by information contained in papers by Colgan (2017: Xenostrobus securis); Colgan et al. (2020: Xenostrobus neozelanicus and X. securis); Horikoshi & Okamoto (2007: X. securis); Iwasaki (2013: X. securis); Iwasaki & Yamamoto (2014: X. securis); Kimura (1996: Vignadula atrata); Kimura et al. (1999: X. securis [?], as Xenostrobus sp.); Lee & Morton (1985: Vignadula mangle comb. nov., as Xenostrobus atratus); Lamarck (1819: X. securis [?], as Mytilus securis; MNHN-IM-2000-34894, three syntypes); Lutaenko et al. (2019: V. atrata); Morton (1999: Xenostrobus pulex); Morton (2004: Xenostrobus inconstans); Morton & Leung (2015: X.securis); Park et al. (2017: V. atrata);Wang et al. (2011: V.atrata); Wilson (1967: Xenostrobus spp.).