Spirobranchus giganteus ( Pallas, 1766 )

Brandão, Ivison Cordeiro & Brasil, Ana Claudia dos Santos, 2020, On a new species of Spirobranchus Blainville, 1818 (Annelida: Serpulidae) and considerations on the genus along the Brazilian coast, Papéis Avulsos de Zoologia 60, pp. 1-17 : 7-9

Spirobranchus giganteus ( Pallas, 1766)

( Figs. 5 , 8 , 9 )

Serpula gigantea Pallas, 1766 .

Spirobranchus (Cymospira) giganteus ( Pallas, 1766) . Blainville, 1828.

Olga elegantissima Jones, 1962 .

Spirobranchus giganteus giganteus ( Pallas, 1766) . ten Hove (1970).

Spirobranchus giganteus . ten Hove (1994); Bastida-Zavala (2009); Bastida-Zavala & Salazar-Vallejo (2000).

Examined material: 29 specimens. Brazil: Alagoas state, Marechal Deodoro Municipality: Frances sandstone reef: 09°46′16.02″S, 35°50′18.57″W, MNRJP-002778 (4 specimens). Saco da Pedra sandstone reef: 09°44′38.20″S, 35°49′08.71″W, MNRJP-002779 (16 specimens). Bahia state: Abrolhos Archipelago, Siriba Island: 17°58′07″S, 38°42′46″W, 3 m, IBUFRJ 0007 (7 specimens). Revizee/ score-Central Project 17°02′31.20″S, 37°36′28.79″W, 50 m, IBUFRJ 3140 (4 specimens). Espírito Santo state: Revizee/score-Central Project 20°09′03.59″S, 37°28′47.99″W, IBUFRJ 3139 (2 specimens). Panama: 34 specimens. Caribbean Sea, San Blás Archipelago: 09°34′37.2″N, 78°53′06″W, 50 m, IBUFRJ 4092 (15 specimens). 09°34′37.20″N, 78°53′60″W, 50 m, IBUFRJ 4093 (10 specimens). 09°34′37.20″N, 78°53′60″W, 50 m, IBUFRJ 4094 (9 specimens).

Diagnosis (modified from Jones, 1962): Operculum possessing two dorsal thorns with prominent spines; mid-ventral thorn often present, smaller, dichotomously branching distally. Radiolar crown arranged in spirals of up to 8 whorls.

Description

Tube: Opaque, white or blueish. Triangular in cross-section, lumen circular. One longitudinal keel along the tube, extending over the opening forming a pointed tip ( Fig. 5B ). Tubes solitary.

Radiolar Crown: Live specimens with irregular bands of coloration, varying from white, beige and blue to pink, yellow, orange or red ( Fig. 5A ), sometimes multiple colors unequally mixed in each lobe; pattern in coloration absent. Coloration faded after preservation, only darker shades remaining. Crown composed of two lobes arranged in spirals with 2-8 whorls, each with up to 200 radioles, basally joined by inter-radiolar membrane for one third of their length ( Figs. 5C, 5D ). Radioles rectangular in cross-section, inner side with two rows off filiform pinnules, distally shorter, with naked tips. Tips filiform and about same size as proximal pinnules. Dorsal radioles longer than ventral ones. Single ocellar cluster forming a compound eye in a dorsal concavity at each of pair of dorsal most radioles.

Mouth Parts: Two thin, smooth lips. Dorsal lips with median notch and forming a pair of lateral filiform palps, about same length as proximal pinnules ( Fig. 5F ).Ventral lip rectangular, forming internal lap along base of radiolar lobes.

Peduncle: Smooth, triangular in cross-section, inserted slightly left to crown midline. Pair of smooth lateral wings forming near base of peduncle, rectangular, with rounded edge, not extending beyond operculum ( Fig. 5C ). Constriction at base of operculum absent. Coloration pattern usually not extending into the lateral wings, but often with vertical bands along opercular rim.

Operculum: Continuous with the peduncle. Opercular ampulla flat, circular in top view, with flat calcareous endplate, generally white, also circular when seen from the top. Two horn-like, symmetrical thorns originating at center of the endplate and projecting dorsolaterally; spines bearing multiple thorns, some with smaller spines. Single ventral spine often present, branching dichotomously at the distal end, also with thorns ( Fig. 5E ). Talon absent.

Collar and Thoracic Membranes: Three-lobed collar. Dorso-lateral lobes shorter, circular, with entire edges, reaching near proximal region of crown; continuous with thoracic membranes, forming ventral apron covering 2 to 3 abdominal chaetigers. Mid-ventral lobe petaloid, longer than dorso-lateral lobes, with wide, round lateral rim and triangular median rim with pointed tip, often folded medially, inserted between crown lobes. Tonguelets present between dorso-lateral and ventral lobes ( Figs. 9C, 9D ), united to dorso-lateral lobes by circular fold; tonguelets trilobed, with two outer lobes: dorsal outer lobe larger, round, with waved rim, ventral outer lobe also round, smaller than dorsal, with smooth rim; inner lobe half the length of external lobes, circular, with smooth rim ( Fig. 9D ). Collar lobes frequently red, pigmentation extending through anterior thorax.

Thorax: Seven chaetigers. Collar chaetae as Spirobranchus - type and limbate chaetae,disposed in one fascicle ( Figs. 8A, 8B ). After collar, notopodial lobes conical, emerging between thoracic membranes and neuropodia.Thoracic chetae limbate, in three fascicles of different lengths per notopodium ( Fig.8C, 8D ). Neuropodial lobes rectangular, all bearing straight tori of similar size through thorax ( Fig. 5G ). Digitiform cirri present at notopodial base ( Figs. 5H , 8C ). Thoracic uncini saw-shaped, with 19-23 curved teeth, plus gouged anterior-most peg ( Fig. 8E ). Parapodial lobes approaching each other posteriorly, forming a ventral triangular depression. Glandular clusters covering ventral portion of mid-ventral collar lobe, forming one pentagonal and two straight inferior bands, also covering all thoracic neuropodia, except for origin of tori, and in ventral depression, as single ventral glandular pad, spoon-shaped.

Abdomen: Largest analyzed specimen with 125 abdominal segments. Abdomen in entire animals usually five times longer than thorax, with larger anterior chaetigers ( Fig. 5I ), the final third abruptly with densely packed chaetigers.Notopodial uncini smaller than thoracic ones, saw-shaped, with 13-16 teeth plus gouged anterior peg ( Fig. 8F ). Neurochaetae as true trumpet-shaped chaetae, abruptly bent, with 2 distal rows of denticles separated by groove and a filiform lateral projection, serrated by minute teeth ( Fig. 8G ). Ventral shields squared anteriorly and rectangular posteriorly. Glandular clusters present basally to tori. Pygidium bilobed, with terminal anus.

Remarks: The distribution of S. giganteus , previously considered circumtropical, has been questioned lately,as for many other “circuntropical” or “cosmopolitan” annelid taxa ( Nygren, 2014; Hutchings & Kupriyanova, 2018). ten Hove (1970) considered the morphospecies forming the S. giganteus complex as subspecies, but later elevated them to separate complexes, nested within the S. giganteus sensu latu complex ( ten Hove, 1994).Thus, as reported by Fiege & ten Hove (1999), two species complexes are recognized in the Atlantic Ocean, S. polycerus ( Schmarda, 1861) and S. giganteus sensu stricto, this latter consisting of S. giganteus ( Pallas, 1766) , S. incrassatus Mörch, 1863 and S. spinosus Moore, 1923 . However, S. incrassatus and S. spinosus were originally described from the Pacific Ocean and their occurrence in the Atlantic is unlikely; also, the opercula of members in these latter two species are either ornamented with long and slender,often hornlike thorns, or with much smaller structures, pointed and normally thicker, called spines; usually, the thorns have spines along the axis. In S. giganteus there are two slender horn-like thorns and frequently a third thorn, bifurcated near the distal end, whereas those of members of S. incrassatus have two thicker thorns next to a third one, bifurcated near the base. Members of S. spinosus have opercula with five thick and short spines. According to information from the WoRMS database, only specimens from the Caribbean region should be identified as S. giganteus ( Read, 2020) . Apart from the original description ( Pallas,1766)and that provided by Mörch (1863),the main source for identification of S. giganteus is the revision by ten Hove (1994), which does not provide a diagnosis. Instead, the diagnosis of Olga elegantissima , by Jones (1962), is the closest to S. giganteus , since Pallas’s original description (1766). In the present work, since specimens of S. giganteus were identified based on comparisons with several individuals from San Blás, in the Caribbean, and the animals were morphologically identical to those found in Alagoas, Bahia and Espírito Santo, we confirm the presence of this species off Brazilian shoreline.

Spirobranchus giganteus is the only Brazilian species of Christmas-tree-worm, those which radiolar lobes form pine tree-shaped spirals. Moreover, the notopodial cirrus found on thoracic chaetigers of our members of this species has not been described for any other species of serpulids. The presence of special collar chaetae and opercular ornamentation distinguish members of S.giganteus from specimens of S. minutus and S. lirianeae sp. nov., in which both these characters are absent.The most similar species to S.giganteus in Brazil is S. tetraceros , with which it was previously synonymized ( Dew, 1959). Brazilian specimens of S. tetraceros were actually identified as belonging to S. giganteus by Skinner et al. (2012), in part of the material used for that study, but that mistake was corrected by Perry et al. (2017). The operculum of specimens of S. tetraceros has a conical endplate, or up to four branched concentric thorns ( ten Hove, 1970; Rodrigues et al., 2020), whereas that of members of S. giganteus has two dorsolateral thorns and, frequently, a bifurcated mid-ventral thorn. Furthermore, whereas animals belonging to S. giganteus have individual compound eyes at the base of each dorsal-most radiolus, members of S. tetraceros only have simple ocelli scattered along the radioles and they present interradiolar processes, which are absent among members of S. giganteus .

Type-locality: Curaçao, Caribbean Sea (Atlantic Ocean).

Habitat: Intertidal: associated to scleractinian corals (Cnidaria: Anthozoa: Scleractinia ) and Milleporidae hidrocorals (Cnidaria: Hydrozoa); rarely found without coral association ( Skinner et al., 2012).

Distribution: Atlantic Ocean: Gulf of México, Caribbean Sea and Brazil, in the states of Pernambuco ( Zibrowius, 1970), Alagoas ( Correia & Sovierzoski, 2009), Bahia ( Rullier &Amoureux,1979; Santa-Isabel et al., 2000), Rio de Janeiro ( Skinner et al., 2012) and Espírito Santo (present paper).

Figures

Figure 5. Spirobranchus giganteus (MNRJP-002778). (A) entire worm, inside fragment of tube, lateral view, (B) anterior end of tube, (C) operculum and radiolar crown,dorsalview,(D)same as C,ventral view,(E) operculum,superior view,(F) base of crown,exposing oral palp,(G) thorax,ventral view,stained withmethylene blue,(H) thoracicnotopodia,(I)anterior abdominal chaetigersScale bars= 1 mm(A,B,C,D,E,G),0,3 mm(I), 0,2 mm (H), 0,1 mm (F).lk= longitudinalkeel.Arrows pointingthe oral palp (F) and parapodial cirri (H).

Figure 8. SEM images of chaetae from species of Spirobranchus reported in Brazil. (A-G) S. giganteus (MNRJP-002779): (A) collar chaetae, (B) detail of shaft of Spirobranchus-type chaeta, (C) thoracic notopodia, (D) limbate thoracic notochaetae, (E) thoracic uncini, (F) abdominal uncini, (G) abdominal trumpet-shaped neurochaetae;(H-K) S. minutus (MNRJP-002785): (H) limbate thoracic notochaetae,(I) thoracic uncini, (J) abdominal uncini, (K) abdominal trumpet-shaped neurochaetae (lateral projection broken); (L-Q) S. tetraceros (MNRJP-002789): (L) collar chaetae, (M) thoracic notopodium,(N) detail of limbate thoracic notochaetae, (O) thoracic uncini, (P) abdominal uncini, (Q) abdominal trumpet-shaped neurochaetae. Scale bars = 500 µm (C), 200 µm (A, M), 100 µm (D, L), 20 µm (N, Q), 10 µm (B, E, F,G,H,K,O,P), 5 µm (I), 2 µm (J).lc = limbate chaeta;pc = parapodial cirrus;sc =Spirobranchus-type chaeta.

Figure 9. Tonguelets among members of Spirobranchus spp. (A, B) S. lirianeae sp. nov.: (A) Paratype (MNRJP-002775) peduncle and dorso-lateral collar lobes dissected, (B) Paratype (MNRJP-002777) detail of the bilobed tonguelet; (C, D) S. giganteus (MNRJP-002779): (C) dorsal view, (D) dorsal view with dorsal outer lobe folded backwards, exposing inner lobe; (E, F) S.minutus (MNRJP-002783): (E) lateral view, (F) detail of tonguelet, dorsal view, stained with Shirlastain,with dorso-lateral collar lobedissected;(G,H)S.tetraceros (MNRJP-002789):(G) lateral view,(H) detail of lateral view stained with methylene blue,outerlobe over inner lobe. Scale bars = 300 µm (G), 200 µm (A, C, D, H), 150 µm (B), 100 µm (E), 50 µm (F). dol = dorsal outer tonguelet lobe; dl = dorsolateral colar lobe; il = inner tonguelet lobe;ol = outer tonguelet lobe;p = peduncle;vol = ventral outer tonguelet lobe.