Stephanotheca, Reverter-Gil, Oscar, Souto, Javier & Fernández-Pulpeiro, Eugenio, 2012

Reverter-Gil, Oscar, Souto, Javier & Fernández-Pulpeiro, Eugenio, 2012, A new genus of Lanceoporidae (Bryozoa, Cheilostomata), Zootaxa 3339, pp. 1-29 : 2-5

Genus Stephanotheca n. gen.

Diagnosis. Colony encrusting, unilaminar to multilaminar. Autozooids densely perforated; marginal areolae in older zooids. Primary orifice with a poorly defined sinus flanked by serrated condyles. No oral spines. Small uniporous septula. Median adventitious avicularium. Rarely vicarious avicularia. Ovicell hyperstomial (i.e. prominent) to subimmersed, or even endozooidal; calcified ectooecium smooth, with a central area of relatively large, often irregularly sized ectooecial pseudopores, surrounded by a nodular crown of imperforate secondary calcification produced by one or more distal zooids; occasionally the entire ectooecium may be covered apart from the perforations. Primary orifice of ovicelled maternal zooids dimorphic, being larger, more rounded and with a shallower sinus than in non-ovicelled zooids. Ovicell opening formed by the concave proximal margin of the ooecium, overarching the primary orifice, and extending to its proximolateral corners; ovicell cleithral. Ancestrula possibly tatiform.

Type species: Stephanotheca barrosoi n. sp.

Etymology. From Greek τέφαν⁰ς (stephanos = crown) and θήκη (theke = box), alluding to the nodular crown of calcification in the frontal surface of the ovicell. Gender feminine.

Discussion. The genus Stephanotheca seems to share some characters with different genera placed in the family Bitectiporidae MacGillivray, 1895 but also with the family Lanceoporidae Harmer, 1957 . This later family is nowadays placed in the superfamily Schizoporelloidea (see Gordon 2011; Bock & Hayward 2012b), but owing to their ‘smittinoid’ ovicells (A. Ostrovsky, pers. comm. February 2012), the Lanceoporidae are here transferred to the superfamily Smittinoidea. The overall appearance of the autozooids of Stephanotheca is similar to many species of Schizomavella and Calyptotheca Harmer, 1957 . These genera also exhibit sinuate orifices, autozooids with frontal shields that are uniformly perforated by small round pseudopores, suboral adventitious avicularia, and enlarged marginal areolar pores that are more defined in older zooids.

The ooecium in Stephanotheca is formed by the distal zooid in its proximal part, and the slit-like coelomic cavity of the ooecium communicates with the cavity of the ooecium-producing zooid via a central pore ( Fig. 1 ). The calcification of ectooecium grows a bit faster ( Figs 2 , 26 ) than calcification of entooecium ( Figs 3, 4, 7 centre zooid, 31, 39, 60). Once the ooecial floor (horizontal part of entooecium) is formed, the lateral (vertical) walls begin to rise ( Fig. 4 centre), formed by entooecium, ectooecium and external, imperforate, secondary calcification, all at the same time. When these three walls begin to form the ooecial roof, encroachment of secondary calcification ceases, forming the nodular crown, while the ectooecium and entooecium still continue, and the former produces the perforated central area ( Figs 5 , 46 ); the rest of the ectooecium seems to be imperforate (see the proximal area in Fig. 5 , and the partially broken ovicell in Fig. 7 , right); consequently, the central perforated area is not only that part of the ectooecium that is uncovered but an actual circumscribed area of perforations beyond which there are none. These perforations in the ectooecial skeleton are sealed in life by cuticular plugs (see Figs 24 , 39 , 67 ) and are visible as true pores in cleaned colonies. These structures will be called pseudopores throughout this paper, but this does not imply homology with frontal-shield pseudopores. The merging of the lateral lobes of the proximal part of ectooecial calcification forms a central suture above the orifice ( Fig. 6 ). In some cases, secondary calcification also covers this proximal area, producing then a complete, circular nodular crown, later perhaps projecting distally into the perforated area ( Fig. 10 ) but normally the secondary calcification produces only thin ridges across the central area that do not occlude the pseudopores so that the central area and the nodular crown remain distinct ( Figs 8 , 47 , 56 ). Additionally, the ovicell can be covered by secondary calcification encroaching from neighbouring zooids ( Figs 32 , 65 ). We have never seen an ooecium without secondary calcification. The whole is formed simultaneously, and probably quite quickly inasmuch as completed ovicells dominate and intermediate stages are relatively few. The first phase (formation of the ooecial floor) also seems to be relatively frequent in occurrence whereas the intermediate phase in which the lateral walls develop is relatively infrequently and would also appear to happen quickly.

The ovicell of the genus Stephanotheca exhibits a structure similar to other genera of the superfamily Smittinoidea (D.P. Gordon, pers. comm. January 2010), and especially it is almost identical to the ovicell in the genera Schizomavella and Hippoporina : a thinly calcified endooecium and a strongly calcified, smooth ectooecium with an exposed area of irregular pseudopores. In the genus Stephanotheca these are located in the rounded central area, surrounded by a nodular crown of secondary calcification ( Figs 9, 10 ) formed by the distal zooid(s). In some cases, this crown can be interrupted in its proximal part in such a way that the smooth frontal area of the ooecium free of calcification elongates towards the zooecial orifice; in this part, it is possible to notice the presence of a longitudinal suture in the entooecium, clearly visible through the ectooecium by light microscopy ( Fig. 6 ).

On the other hand, the double-walled structure of the ooecia in Stephanotheca is basically the same as in genera of Lanceoporidae (e.g. Calyptotheca , Emballotheca Levinsen, 1909 and Parmularia MacGillivray, 1887 ), except that secondary calcification overgrows the entire ooecium in some lanceoporid species. In this family, secondary calcification tends to be cormidial, i.e. produced by adjacent zooids according to a strict pattern, with sutures sometimes forming a Y; the secondary calcification is also perforated, by pseudopores that are in correspondence with the pseudopores in the ectooecium. In Hippoporina ussowi ( Kluge, 1908) , the secondary calcification is produced by 2–3 distal zooids, often forming a Y as in Lanceoporidae ; it also totally covers the ectooecium but, in contrast with Lanceoporidae , it is imperforate, occluding then the ectooecial pseudopores (A. Ostrovsky, pers. comm. February 2012). Nevertheless, the systematic position of this species is uncertain, since the presence of a suboral avicularium and the structure of the ovicell preclude placement in the genus Hippoporina . In Stephanotheca , although the ooecial cover can be formed by several zooids ( Figs 32 , 65 ) the pattern is quite chaotic, and only sometimes with raised sutures over the ovicell. The secondary calcification on the lateral walls of the ooecium is also imperforate, as with the underlying ectooecium. Insofar as the central area of ectooecium in Stephanotheca can also be covered by ridges of secondary calcification that do not occlude the pseudopores there is no structural difference between this genus and the Lanceoporidae ; it is just a matter of the extent of both the perforated ectooecial area, and the cover of secondary calcification ( Figs 47 , 56 ).

The species here included in Stephanotheca n. gen. were previously placed in Schizomavella . The primary orifice of Stephanotheca lacks articulated oral spines, and has a poster with a wide, poorly defined sinus owing to rounded and sloping margins, flanked by condyles that are denticulate in all but in one species. The overall character of the orifice differs from that in Schizomavella , in which spines may be present, the poster is transverse and the sinus often exhibits well-defined corners, while few species have denticulate condyles.

The most important feature, however, that distinguishes the present genus from Schizomavella , as well as from Hippoporina , is the shape of the ovicell opening and its closure. In the original generic diagnosis of Schizomavella, Canu & Bassler (1917) stated that the operculum closes the ovicell opening, but later authors have sometimes overlooked or ignored this character. However, we believe that Canu, at least, did not really know the species S. auriculata — of 17 samples labelled S. auriculata in his collection in MNHN, 15 of them correspond to other species of the genus, mostly Schizomavella cornuta ( Heller, 1867) . Only two, from the north of France, were actual S. auriculata but were labelled as ‘varieties’ (systolostoma and reticulata). This confusion generally prevailed until Hayward & Thorpe (1995) redescribed S. auriculata , and selected a neotype. These authors stated that in this genus the ovicell is not closed by the operculum although in their figures this detail was not documented. Thus, this question was resolved years ago but it did not have the deserved impact.

Based on our own material, which is identical to the neotype of S. auriculata (NHMUK 1911.10.1.1533) that we examined years ago (Reverter-Gil & Fernández-Pulpeiro 1995), the ovicell in these species is indeed acleithral ( Figs 11, 12 ). The opening of the ovicell, closed by the ooecial vesicle in life, is very narrow, deeply immersed and not easily seen directly, except for its lower lip. This arrangement is the same in other species of Schizomavella sensu stricto (personal observations and A. Ostrovsky, pers. comm. January 2010). Moreover, dimorphic orifices are absent from Schizomavella and also Hippoporina , a bitectiporid genus with cleithral ovicells.

In contrast, in the species assigned here to Stephanotheca , the ovicell is closed by the operculum and maternal zooids have a dimorphic primary orifice with a wider, shallower sinus than in non-ovicellate zooids. The opening of the ovicell is formed by the concave proximal ooecial margin that overarches the primary orifice, extending to its proximolateral corners ( Figs 9, 10 ), with the primary orifice of the autozooid set just below the ovicell opening ( Figs 5 , 16 , 24 , 29 , 35 , 44 , 65 ). In some dried uncleaned colonies, the opening of some ovicells is closed by the zooidal operculum, while in others the operculum is lowered onto the distal margin of the primary orifice. There is, however, the possibility that we are dealing with a variant of the subcleithral type. In both types, ovicell closure is achieved by the combination of the non-calcified distal wall of the maternal zooid (sometimes protruding into the brooding cavity and forming the ooecial vesicle) and the zooidal operculum (A. Ostrovsky, personal communication, January 2012; see Ostrovsky 2008, fig. 4E). In the cleithral type the ovicell is opened by raising the zooidal operculum during larval release, whereas in the subcleithral one an ovicell is opened by the lowering of the operculum — in this instance the tentacular crown is retracted during larval release. As soon as a larva leaves the ovicell, the operculum is correspondingly lowered or raised and closes its opening again. In dried specimens of both cleithral and subcleithral types the operculum often lowers and closes the zooidal primary orifice because of tissue collapse; therefore, ovicell closure in Stephanotheca would be cleithral when alive. Detailed definitions of cleithral, acleithral and subcleithral and their functional significance can be found in Ostrovsky (2008) and Ostrovsky et al. (2009).

On the other hand, the orifice of Stephanotheca is also similar to that in some species of Calyptotheca , as for instance Mediterranean Calyptotheca rugosa Hayward, 1974 and C. obscura Harmelin et al., 1989 . In these species, however, as well as in others of the genus, the distal rim of the orifice has an inner shelf-like platform (lunula) on which the operculum rests when closed. Ovicell closure in Stephanotheca is closely similar to that in Calyptotheca , as can be also be seen in fossil species of the genus such as Calyptotheca sp. 1 and Calyptotheca sp. 2 reported by Berning (2006).

In Stephanotheca barrosoi n. sp., the type species of the genus, some zooids have an extremely elongated orifice ( Figs 13, 17–20, 23 ). They were depicted in a figure by Barroso (1923, 1935) that was later reproduced by Zabala (1986: 479, fig. 164A). This type of zooid can be considered as a less-derived form of vicarious avicularium (see Harmelin et al. 1989). This type of avicularium, otherwise little known in the Bitectiporidae [cf. Schizosmittina (Gordon 1984, pl. 33E)], is similar to that in Calyptotheca obscura and in some species of Parmularia MacGillivray, 1887 , such as P. quadlingi ( Haswell, 1880) and P. occidenta Chimonides & Cook, 1993 . Harmelin et al. (1989) pointed out the relationship between Calyptotheca and, among others, Schizomavella , based on the presence of a vicarious avicularium in Schizomavella inclusa ( Thornely, 1906) and in S. ambita as cited by Barroso (1935). However, the former species is now placed in Calyptotheca , as suggested by the authors ( Harmelin et al. 1989: 301), while Barroso’s record (1935) is here considered as corresponding to the type species of Stephanotheca .

We consider that the group of species described here has enough morphological identity as to constitute a separate genus. Notwithstanding, without SEM, zooidal characters do not always allow for clear differentiation from genera such as Schizomavella or Calyptotheca . In fact, the limits of these genera are still blurred, such that several species of the latter were previously ascribed to Schizomavella , while, in contrast, Calyptotheca triarmata Hayward, 1974 is now considered to be a junior synonym of Schizomavella asymetrica ( Calvet, 1927) (see Hayward & McKinney 2002). However, we consider that the shape and position of the ovicell opening and the type of ovicell closure are consistent enough to allow for the definition of a new, distinct genus for the species described below. All of them exhibit a very uniform appearance, which makes their differentiation very difficult without SEM. The most useful diagnostic features are 1) the frequency, size, shape and position of the suboral avicularium and 2) the extent of the exposed pseudoporous area of the ooecium and the development of the nodular secondary calcification surrounding it (although ovicells are not always present in available material). Other useful diagnostic characters comprise features that are hard to resolve without SEM, such as the shape and denticulation of the orificial condyles.

The affinities of Stephanotheca within the superfamily Smittinoidea are somewhat equivocal as the genus shares several characters with different taxa in the families Bitectiporidae and Lanceoporidae . On the one hand, the structure of the ovicell is almost identical to that in Schizomavella and Hippoporina , but these genera lack dimorphic orifices. Also zooids with enlarged orifices that appear to be ‘primitive’ or less-derived vicarious avicularia are rare in the Bitectiporidae . On the other hand, ovicell structure is not qualitatively different from that in the Lanceoporidae , in which secondary calcification covers the ooecium and may be contributed cormidially by adjacent zooids but does not occlude the perforations in the ectooecium. Also many species of Calyptotheca have dimorphic orifices and vicarious avicularia. The choice of family for Stephanotheca depends on whether these characters are considered as analogous structures, owing to convergent evolution, or homologous, as well as on the weight assigned to each character. Without gene-sequence data, these decisions are presently subjective.

The structure of the ovicell is of course an important character for the classification of the species, but as stated above, the ovicell of Stephanotheca , closely similar to that in Bitectiporidae , cannot be considered different from the Lanceoporidae . In fact, the ‘smittinoid’ ovicells are widespread among both umbonulomorph and lepraliomorph genera (A. Ostrovsky, unpublished data). Dimorphic orifices and cleithral ovicells are rather common characters and may be connected with each other. This combination evidently evolved independently several times in cheilostomes (A. Ostrovsky, pers. comm. February 2012) and may not be supportive of close relationships among disparate taxa. Such is likely also to be the case with the putative vicarious avicularium. Taking all of the characters into consideration we provisionally place Stephanotheca in the Lanceoporidae . Additionally, the sharing of the morphological characters of Stephanotheca with the Bitectiporidae and Lanceoporidae reinforces the placement of Lanceoporidae within the Smittinoidea.

Stephanotheca can be distinguished from Calyptotheca by the more reduced, non-perforate secondary calcification of the ovicells, leaving a central pseudoporous area of ectooecium; in contrast, pseudoporous secondary calcification entirely overgrows the perforated ectooecium in Calyptotheca . Parmularia ( Lanceopora in some accounts) differs in having erect bilaminate colonies supported by a rooted kenozooid, as well as a lack of adventitious avicularia; it shares sutured cormidial secondary calcification of the ovicell with some species of Calyptotheca . Emballotheca has orifices without a sinus.

Figures

FIGURES 1 – 8. Ovicell development in Stephanotheca. 1, communication pore between the ooecium-producing zooid and the coelomic cavity of the ooecium (arrow) (S. barrosoi n. sp.). 2, calcification of ectooecium and beginning of the calcification of entooecium (S. watersi n. sp.). 3, calcified ooecial floor (S. ochracea n. comb.). 4, developing ooecia (S. watersi n. sp.). 5, developing ooecium (S. monoecensis n. comb.). 6, central suture of the ectooecium (arrow) (S. barrosoi n. sp.). 7, complete ovicell, ooecial floor, and a partially broken ovicell showing ectooecial pseudopores (S. watersi n. sp.). 8, secondary calcification growing over the central porous area (S. monoecensis n. comb.).

FIGURES 26 – 30. Stephanotheca watersi n. sp. 26, view of the colony with developing ooecia (paratype: MNHN 11148); 27, primary orifice (holotype: MM 2845); 28, primary orifice (paratype: MNHN 11141); 29, same, two ovicellate zooids; 30, view of the colony (holotype: MM 2845).

FIGURES 45 – 49. Stephanotheca monoecensis (Calvet, 1927) n. comb. 45, view of a colony (MNHN 2378); 46, developing ovicell and subtriangular avicularia (MNHN 11192); 47, ovicellate and non-ovicellate zooids with two different avicularia (photo by J. - G. Harmelin); 48, primary orifice (MNHN 11151); 49, primary orifice (MNHN 2378).

FIGURES 24 – 25. Stephanotheca ambita (Waters, 1889) n. comb. 24, ovicellate and non-ovicellate zooids (lectotype: MM 2938); 25, primary orifice (paralectotype: MM 2936).

FIGURES 36 – 39. Stephanotheca ochracea (Hincks, 1862) n. comb. (holotype: NMHUK 1899.5.1.977). 36, zooids with gigantic avicularia; 37, primary orifice and small suboral avicularium; 38, primary orifice; 39, ovicellate zooids.

FIGURES 62 – 67. Stephanotheca arrogata (Waters, 1879) n. comb. 62, view of the colony with ovicellate zooids (lectotype: MM 2852); 63, same, primary orifice; 64, same, autozooids with avicularia; 65, same, ovicellate and non-ovicellate zooids; note the cormidial secondary calcification covering the ovicells, contributed by several zooids; 66, same, ovicellate zooid; 67, view of the colony with ovicellate zooids (paralectotype: MM 2969).

FIGURES 9 – 10. Ovicell in Stephanotheca (S. barrosoi n. sp.). More information in the text. nc: nodular crown; oa: ovicell opening; pa: pseudoporous area; po: primary orifice.

FIGURES 50 – 56. Stephanotheca triangulata n. sp. 50, view of the colony (holotype: NHMUK 1899.7.1.2342); 51, same, autozooids; 52, same, primary orifice; 53, primary orifice and avicularium (paratype: NHMUK 1939.7.4.12); 54, autozooids (paratype: NHMUK 1899.7.1.2346); 55, same, view of the colony with ovicellate zooids; 56, broken ovicells (holotype: NHMUK 1899.7.1.2342).

FIGURES 31 – 35. Stephanotheca victoriensis n. sp. 31, view of the colony with developing ooecia (paratype: MM 4172); 32, same, autozooids and developing ooecium; note the raised sutures growing over the ovicell; 33, same, primary orifice of ovicellate zooid; 34, same, primary orifice; 35, view of the colony with ovicell (holotype: MM 2937).

FIGURES 11 – 12. Schizomavella auriculata (Hassall, 1842) (Ría de Ferrol). 1, maternal zooid with ovicell and operculum closing primary orifice. 2, inner view of a broken ovicell, showing secondary calcification covering ectooecium and partial entooecium. Primary orifice of the maternal zooid is seen below the proximal margin of the ovicell.

FIGURES 13 – 19. Stephanotheca barrosoi n. sp. (holotype: MNCN 3829). 13, general view, with ovicells and a vicarious avicularium; 14, primary orifice. 15, autozooid with a suboral avicularium; 16, maternal zooid and ovicell; 17, vicarious avicularium; 18, vicarious avicularium with operculum. 19, vicarious avicularium with suboral avicularium.

FIGURES 40 – 44. Stephanotheca monoecensis (Calvet, 1927) n. comb. (lectotype: MOM 42 - 1421). 40, view of the colony; 41, primary orifice; 42, primary orifice and central avicularium; 43, ovicellate zooid. 44, view of the colony with autozooids and ovicellate zooid.