Exocoelactinidae Carlgren, 1925

Yanagi, Kensuke, Fujii, Takuma & Hirose, Mamiko, 2015, Redescription of the Sea Anemone Exocoelactis actinostoloides (Cnidaria: Anthozoa: Actiniaria) Based on a Topotypic Specimen Collected from Tokyo Bay, Japan, Species Diversity 20, pp. 199-209 : 200-206

Family Exocoelactinidae Carlgren, 1925 Genus Exocoelactis Carlgren, 1925

Exocoelactis actinostoloides ( Wassilieff, 1908) [New Japanese Name, Dofurain-isoginchaku] ( Figs 2–7 ; Table 1)

Cymbactis actinostoloides Wassilieff, 1908: 25 , figs 10–11; pl. II, fig. 24; pl. VII, figs 74–75 (type locality: Jogashima , Sagami Bay, Japan) .

Cymbactis maxima Wassilieff, 1908: 27 ; pl. II, fig. 25; pl. VII, figs 76–80, (type locality: Enoshima , Sagami Bay, Japan) .

Exocoelactis valdiviae Carlgren, 1928: 187 , pl. III, fig. 1; textfigs 32, 33.

Parasicyonis actinostoloides ( Wassilieff, 1908) : Carlgren 1921: 208.

Parasicyonis maxima ( Wassilieff, 1908) : Carlgren 1921: 208.

Parasicyonis (Cymbactis) actinostoloides ( Wassilieff, 1908) : Carlgren 1949: 80.

Parasicyonis (Cymbactis) maxima ( Wassilieff, 1908) : Carlgren 1949: 80.

Parasicyonis actinostroides (sic) ( Wassilieff, 1908): Uchida and Soyama 2001: 154 (listed).

Parasicyonis (?) (sic) maxima ( Wassilieff, 1908) : Uchida and Soyama 2001: 154 (listed).

Exocoelactis actinostoloides ( Wassilieff, 1908) : Arellano and Fautin 2001: 648, figs. 1–6 ( New Caledonia, Palau, Philippines, Chesterfield Islands, and Loyalty Islands Basin); Yanagi 2006: 148.

Non Parasicyonis actinostoloides: Uchida, 1965: 267 ; Moyer and Bell, 1976: 24; Cha and Song, 2001: 100.

Non Parasicyonis actinostoroides (sic): Uchida et al. 1975: 31

Non Parasicyonis actinostroides (sic): Suzuki and Hayashi 1977: 198.

Non Parasicyonis maxima: Uchida et al. 1975: 32 .

Non Entacmaea actinostoloides: Uchida 1992: 139 .

Material examined. CMNH-ZG 05926 : female, off Ukishima island , Kanaya , Futtsu city, Chiba Prefecture, in Uraga Strait , mouth of Tokyo Bay, Japan, 100–200 m depth, 24 October 2012, collected by Mamiko Hirose using a fisherman’s gill net ( Fig. 1 ); ZSM 20040087 : (Collection of the State Zoological Museum, Munich) holotype, Jogashima, Sagami Bay, Japan, May 1904, depth uncertain, collected by Frantz Doflein ( Fig. 2 ); ZSM 20040088 : holotype of Cymbactis maxima, Enoshima, Sagami Bay , Japan, May 1904, depth uncertain, collected by Frantz Doflein .

Description. External anatomy ( Fig. 3A–D ): Freshly collected specimen with column creamy white ( Fig. 3B ), oral disc with narrow orange radial stripes on light orange background ( Fig. 3A, C ); tentacles of same color as oral disc background color proximally, orange distally ( Fig. 3A ); oral side of tentacles slightly darker colored than aboral side ( Fig. 3B ). In living, expanded animal, column height 70 mm; oral disc diameter 150 mm, pedal disc diameter 65 mm; pedal disc weakly adherent, circular in outline. Scapus smooth, with no distinct margin or fosse ( Fig. 3D ). Mouth slit-like, raised on cone, with indistinct lip ( Fig. 3C ). Tentacles marginal, short, more or less capitate, simple, shorter than oral disc diameter, inner ones longer than outer, altogether 108 in number (CMNH-ZG 05926). Two siphonoglyphs distinct ( Fig. 3C ).

Mesenteries ( Fig. 4A–C ): Two pairs of directive mesenteries connected to siphonoglyphs. Pairs of mesenteries, 65 in number, arranged as typical for the Exocoelactinidae . Six pairs of mesenteries of 1st and 2nd cycles perfect. Pairs of mesenteries of 3rd cycle complete, fertile, 24 in number, two pairs situated bilaterally in each exocoel of 1st and 2nd cycles. Pairs of mesenteries of 4th cycle incomplete, 24 in number, in exocoels between adjacent pairs of mesenteries of 3rd cycle. Five pairs of mesenteries of 5th cycle without filaments, present in some exocoels between adjacent pairs of mesenteries of 4th cycle. In each pair of mesenteries of 3rd and 4th cycles, mesenteries unequally developed; larger one with its retractor muscle facing towards mesentery of previous cycle.

Histology ( Figs 5A–F , 6A–D ): Marginal sphincter muscle mesogloeal, weak ( Fig. 5A ). Musculature mesh-like with small “alveoli” ( Figs 5B , 6A ). Muscle fibers aligned on inner wall of alveoli as single-layered sheet ( Fig. 6B ). Longitudinal muscle of tentacles and radial muscles of oral disc mesogloeal. Musculature an open mesh with alveoli ( Fig. 5B, C ; 6C, D ). Retractor muscles diffuse, weak ( Fig. 5E ). Parietobasilar muscles diffuse without pennon ( Fig. 5E ). In gonadal area, eggs each with trophonema ( Fig. 5F ).

Cnidae ( Figs 7 , 8 , Table 1): spirocysts, basitrichs, microbasic p -mastigophores. See Table 1 and Fig. 8 for size and distribution.

Distribution. Known from Jogashima, Sagami Bay, Japan (holotype); Enoshima, Sagami Bay, Japan (holotype of Cymbactis maxima ); off Ukishima, Uraga Strait, mouth of Tokyo Bay, Japan (this study); New Caledonia, Palau, and Philippines ( Arellano and Fautin 2001); off coast of Somali Peninsula (syntypes of Exocoelactis valdiviae ). Bathymetric range 175–480 m ( Arellano and Fautin 2001); depth of occurrence of present specimen 100–200 m, with no further information available.

Phylogenetic analysis. We performed phylogenetic analyses using the 16S and 12S rDNA sequences, resulting in a total of 1094 base pairs. The analyses of the concatenated 16S and 12S rDNA showed that Ex. actinostoloides groups within the superfamily Actinostoloidea (see Rodríguez et al. 2014) ( Fig. 9 ). The concatenated phylogenetic tree showed that Ex. actinostoloides forms a highly supported clade with Actinostola Verrill, 1883 and Stomphia Gosse, 1859 (ML=90%, Bayes=0.97).

Figures

Fig. 2. Holotype of Exocoelactis actinostoloides (ZSM 20040087).

Fig. 3. Exocoelactis actinostoloides (CMNH-ZG 05926) from Uraga Strait, mouth of Tokyo Bay, live. A, oral view; B, lateral view; C, oral view around mouth; D, lateral view of upper part of column. s, siphonoglyph. Scale bars (lower right in each image): 20mm.

Fig. 4. Mesenterial arrangement of Exocoelactis actinostoloides (CMNH ZG 05926). A, diagrammatic image; B, gross transverse section of column at level of pharynx; C, histological transverse section of approximately one-third of whole cycle in lower part of column, just under pharynx. Abbreviations: I–V, pairs of mesenteries of first to fifth cycle respectively; d, pairs of directive mesenteries; g, gonad; p, pharynx; s, siphonoglyph. Scale bars:10mm.

Fig. 5. Images of histological sections of Exocoelactis actinostoloides (CMNH ZG 05926). A–B, longitudinal sections of mesogloeal sphincter; C–D, transverse sections of tentacular longitudinal muscle; E, transverse section of mesenterial retractor muscle; F, oocyte with trophonema. Abbreviations: cm, column; ed, epidermis; en, enteron; gd, gastrodermis; gv, germinal vesicle; mf, mesenterial filament; mg, mesogloea; oc, oocytes; pm, parietobasilar muscle; rm, retractor muscle; sm, sphincter muscle; te, tentacle; tm, tentacular longitudinal muscle; tr, trophonema. Arrows in B and D: muscle fibers. Scale bars: 500µm for A, C, E; 50µm for B, D, F.

Fig. 6. Scanning electric microscope images of musculature of Exocoelactis actinostoloides (CMNH-ZG 05926). A, sphincter; B, enlarged detail of A (area within rectangle); C, tentacular longitudinal muscle; D, enlarged detail of C (area within rectangle). Abbreviations: ed, epidermis; gd, gastrodermis; mg, mesogloea; mf, muscle fibers; sm, sphincter muscle; tm, tentacular longitudinal muscle. Scale bars: 200µm for A, C; 10µm for B, D.

Fig. 7. Cnidae from tentacle, column, pharynx, and mesenterial filaments of Exocoelactis actinostoloides (CMNH-ZG 05926). For letters a–m, refer to Table 1. Scale bar: 50µm.

Fig. 1. Localities of Exocoelactis actinostoloides (Wassilieff, 1908) around Sagami Bay, Japan. Jogashima and Enoshima are the type localities of Ex. actinostoloides and Cymbactis maxima Wassilieff, 1908, respectively.

Fig. 8. Size distribution of cnidae of Exocoelactis actinostoloides (CMNH-ZG 05926). Squares indicate ranges of length and width reported by Arellano and Fautin (2001: 654, table 2): orange squares, holotype; green squares, other specimens investigated by Arellano and Fautin (2001). “n” is number of capsules measured. For letters a–m, refer to Table 1 and Fig. 7.

Fig. 9. Maximum likelihood tree of total 1094 base pairs of concatenated 12S rDNA and 16S rDNA, showing placement of newly obtained sequences from Exocoelactis actinostoloides (CMNH-ZG 05926) among previously published GenBank sequences. Values of ML bootstrap values>60% are shown at the respective nodes; monophylies with Bayesian posterior probabilities of>0.90 in Bayseian tree are shown by thick branches. Ex. actinostoloides is shown in a bold and larger font. Species names corresponding to sequences from previous studies are shown in regular font. Black and white stars indicate members of the family Actinostolidae sensu Rodríguez et al. (2008) and Exocoelactinidae, respectively.