Membranipora de Blainville, 1830

Dick, Matthew H., Grischenko, Andrei V. & Mawatari, Shunsuke F., 2005, Intertidal Bryozoa (Cheilostomata) of Ketchikan, Alaska, Journal of Natural History 39 (43), pp. 3687-3784 : 3691-3696

Genus Membranipora de Blainville, 1830

Membranipora villosa Hincks, 1880

( Figure 1A–F )

Membranipora villosa Hincks 1880a, p 84 , Plate 10, Figure 8 .

Membranipora villosa: Robertson 1908, p 269 , Plate 16, Figures 22 , 23 , Plate 17, Figures 24 , 25; O’Donoghue and O’Donoghue 1923, p 26; 1926, p 29; Soule et al. 1995, p 39, Plate 4D.

Membranipora membranacea: Hincks 1882, p 469 ; Robertson 1908, p 267, Plate 16, Figures 19 , 20 ; O’Donoghue and O’Donoghue 1923, p 26; Osburn 1950, p 21, Plate 1, Figures 8 , 9 .

Membranipora membranacea form serrata Hincks 1882, p 469 .

Membranipora serrata: Robertson 1908, p 268 , Plate 16, Figures 20 , 21; O’Donoghue and

O’Donoghue 1923, p 26; 1926, p 29.

Membranipora serrilamella Osburn 1950, p 22 , Plate 1, Figures 12, 13 .

Membranipora serrilamella: Soule et al. 1995, p 39 , Plate 4A, B.

Description

Colony. Unilaminar, encrusting, sheet-like, ranging in size from small, circular, young colonies to large expanses of coalesced colonies on laminarian algae, including plants directly accessible low in the intertidal.

Zooids. Elongate-rectangular, 0.53–1.20 mm long (average 50.849 mm, n 548, 4) by 0.23– 0.41 mm wide (average 50.290 mm, n 548, 4); closely appressed, with a narrow rim between them; walls thin and flexible or more heavily calcified and brittle; basal wall uncalcified. Frontal surface completely covered by membrane; with or without acute, short or long, flexible cuticular spines ( Figure 1C, E ) arising from frontal membrane and along zooidal margins. Cryptocyst lies close below marginal rim, sometimes farther depressed distally; widest around proximal third of zooid and distal end, narrowest in central third; variably developed, consisting of a slight shelf that is smooth or weakly serrate (‘‘ membranacea ’’ form; Figure 1A ), a weakly developed shelf of minute denticles replaced by longer denticles every so often (‘‘ villosa ’’ form; Figure 1D ), or a pronounced shelf with smaller and longer denticles, sometimes with a pronounced denticle in proximal midline (‘‘ serrilamella ’’ form; Figure 1B ). Distal cryptocyst is generally smoother than that more proximally. Distal margin sometimes extended as a raised rim.

Opesia. Differing from shape of zooidal margin by width of narrow cryptocyst; with rightangled corners proximally, or corners rounded at both ends ( Figure 1B shows both cases).

Spines. Zooids have a short, blunt, hollow, conical, spine-like knob at each proximal corner ( Figure 1A, B, D, F ), formed by extension and folding of the marginal wall ( Figure 1D ), with closure of the fold to give a hollow process; sometimes extended with a long, curved, acute, chitinous projection (‘‘ villosa ’’ form; Figure 1C ).

Avicularia. Lacking.

Ancestrula . Not observed.

Remarks

Three morphologically similar species of Membranipora have been reported in the northeastern Pacific: M. membranacea (L.) characterized by a negligible, smooth or finely serrate cryptocyst and lacking frontal cuticular spines; M. villosa Hincks characterized by a finely serrate cryptocyst and having numerous cuticular spines on the frontal membrane and zooidal margins; and M. serrilamella Osburn , characterized by a markedly serrate, spinous cryptocyst and lacking frontal cuticular spines. Yoshioka (1982) argued that these putative species represent a single species, and that the apparent difference among them are due both to ecophenotypic variation, induced partly by the presence of nudibranch predators, and to astogenetic variation. He concluded that M. villosa and M. serrilamella are synonyms of M. membranacea . However, Soule et al. (1995) retained the name M. serrilamella , arguing that it is morphologically distinct from Atlantic M. membranacea ; furthermore, they did not include M. villosa in their synonymy of M. serrilamella and provided separate illustrations of the two.

More recently, a study by Schwaninger (1999) supported Yoshioka’s results with a phylogeny of M. membranacea- and M. villosa -like morphs from Friday Harbour, Washington and M. serrilamella from Japan. Based on 600 base pairs of the mitochondrial COI gene, her phylogeny showed that single mitochondrial lineages include representatives of all three morphs. Furthermore, the three morphs proved to be genetically indistinguishable at the allozyme level, with no fixed allelic differences among them and low H values, indicating free gene flow. Schwaninger thus concluded that the three morphs are conspecific. Unfortunately, she did not show SEM illustrations of the specific morphologies included in her phylogeny. Her definition of non-‘‘ serrilamella ’’ morphs depended on the presence or absence of frontal cuticular spines, without reference to the nature of the cryptocyst, which has also been a key character in distinguishing among the nominal species reported from the north-eastern Pacific.

There is general agreement among these recent studies that M. membranacea (L.) does not occur in the north-eastern Pacific. Yoshioka (1982) noted that the cyphonautes of European M. membranacea is larger and differently ornamented than the cyphonautes attributed to the ‘‘ membranacea ’’–‘‘ serrilamella ’’–‘‘ villosa ’’ morphs in the northeastern Pacific. Schwaninger (1999) found an average COI divergence of 13% between North Atlantic and North Pacific populations of nominal M. membranacea , and concluded that these regions ‘‘harbor highly differentiated populations of M. membranacea -like morphs that may no longer belong to the same species’’. Schwaninger also noted, ‘‘there were no obvious differences in adult morphology between these populations’’, and continued to refer to Pacific populations as M. membranacea . However, Soule et al. (1995) observed differences in zooid morphology between M. membranacea they examined in France and M. serrilamella in the eastern Pacific, and concluded that these are distinct species.

At Ketchikan, we found colonies identifiable with ‘‘ membranacea ’’-like ( Figure 1A ) and ‘‘ serrilamella ’’-like ( Figure 1B ) morphologies, both lacking frontal cuticular spines. These are similar to one another in all respects except degree of development of the cryptocyst; the former has a negligible, faintly serrated cryptocyst, whereas the latter has a highly denticulate cryptocyst with long denticles interspersed with more numerous shorter ones. We also found a ‘‘ villosa ’’-like morph, with thinner, less heavily calcified walls having a weakly denticulate cryptocyst ( Figure 1D ), and frontal cuticular spines ( Figure 1C ). Another ‘‘ villosa ’’-like specimen we examined from Sitka, Alaska has abundant long, frontal cuticular spines ( Figure 1E ) and more heavily calcified walls than the Ketchikan specimen, yet also shows a ‘‘ serrilamella ’’-like cryptocyst ( Figure 1F ). The two ‘‘ villosa ’’-like morphs have in common a raised distal rim not present in the other morphs, but this may be an ecophenotypic character, either inducible by nudibranch predators in the same manner as the cuticular spines, or correlated with subtidal habitat. The two ‘‘ villosa ’’-like specimens encrusted laminarian algae continually submerged in a boat harbour, whereas the other morphs encrusted nearshore laminarian algae subject to wave action.

We conclude, from examining admittedly a limited number of specimens from southeastern Alaska, that there is no suite of characters that can consistently distinguish among the morphs previously reported as separate species in the north-eastern Pacific. Other authors have mentioned similar observations. For example, O’Donoghue (1926) noted, in reference to M. villosa , M. serrilamella , and M. membranacea , ‘‘A colony of one … may contain an area which, if found by itself, might easily be referred to the other’’. Similarly, Yoshioka (1982) noted, ‘‘…characteristics of all three species can be found in different parts of a single colony’’. It is also noteworthy that Osburn (1950) reported the ranges of the three nominal species in the eastern Pacific as virtually identical, from British Columbia to Southern California, with the exception of Robertson’s (1900) records of nominal M. membranacea from Yakutat and the Pribilof Islands, Alaska. Here, we consider the ‘‘ membranacea ’’, ‘‘ villosa ’’, and ‘‘ serrilamella ’’ morphs in the north-eastern Pacific as synonymous, yet distinct from European M. membranacea (L.). Nomenclatural priority therefore goes to M. villosa Hincks, 1880 , the earlier description in the eastern Pacific of either of the two morphs ( M. serrilamella and M. villosa ) other than M. membranacea .

We note, however, that questions remain concerning the identity of Membranipora spp. in the north-eastern Pacific. For instance, Osburn (1950, p 21, Plate 1, Figure 9 ) noted the presence and included an illustration of ‘‘tower cells’’ for nominal M. membranacea from the Pacific. These tower zooids are characteristic of European M. membranacea (L.) ( Hayward and Ryland 1998), and their presence suggests the occurrence of that species in the Pacific, perhaps as an introduced population. Also troublesome are the deep (up to 17%) divergences in three COI lineages within a Membranipora population at a single locality, Friday Harbour, Washington ( Schwaninger 1999); these divergences are greater than that (13%) between Atlantic and Pacific populations. It is also interesting to note that although M. serrilamella has been reported from Japan ( Mawatari 1974), M. villosa has not. If the two were simply morphs of the same species, one would expect to find both in Japan. However, lack of the villosa morph there might be explained by absence ( Okutani 2000) of the specific nudibranch predators, Doridella steinbergae Lance and Corambe pacifica MacFarland and O’Donoghue ( Yoshioka 1982) , that induce chitinous frontal spines in eastern Pacific populations. This would make sense if M. serrilamella had been introduced to Japan from the eastern Pacific, in which case Japanese populations of nominal M. serrilamella might not exhibit a defensive response to chemical cues from species of nudibranch predators native to Japan. An introduction would also explain the low genetic divergence between Japanese specimens and one of the clades at Friday Harbour, Washington ( Schwaninger 1999). Ultimately, integrated morphological, ecological, and molecular genetic studies will be necessary to resolve the taxonomy of Membranipora in the northern Pacific.

Distribution

Pribilof Islands and Yakutat, Alaska (as M. membranacea ) ( Robertson 1900) southward to southern California ( Robertson 1908; O’Donoghue and O’Donoghue 1923, 1926; Osburn 1950); southern Hokkaido (as M. serrilamella ) ( Mawatari and Mawatari 1981) southward to Wakayama Prefecture on the Pacific side and Ishikawa Prefecture on the Sea of Japan, Honshu, Japan (as M. serrilamella ) ( Mawatari 1974).

Suborder NEOCHEILOSTOMINA d’Hondt, 1985

Figures

Figure 1. Membranipora villosa Hincks. (A) ‘‘Membranacea’’ form, weakly bleached; (B) ‘‘serrilamella’’ form, bleached; (C) ‘‘villosa’’ form; unbleached; note acute chitinous spines at proximal corners and cuticular spines on frontal membranes; (D) ‘‘villosa’’ form; same colony as (C) after bleaching, showing weakly denticulate cryptocyst; (E) ‘‘villosa’’ form from Sitka, Alaska; weakly bleached specimen with zooids showing both denticulate cryptocyst and cuticular spines on frontal membrane; (F) ‘‘villosa’’ form from Sitka, Alaska; same colony as (E), with zooids showing coarse, highly denticulate cryptocyst. Scale bars: 500 Mm (A–C, E, F); 400 Mm (D).

Figure 8. (A–D) Puellina caesia n. sp.: (A) group of autozooids; bleached; (B) group of ovicellate zooids; bleached; (C) colony margin showing several stages of ovicell formation; bleached; (D) enlargement showing setiform papillae proximolateral to orifice; unbleached. Scale bars: 400 Mm (A); 500 Mm (B, C); 200 Mm (D).

Figure 9. Celleporella hyalina (L.) species complex, showing variation between two colonies encrusting a single mussel (Mytilus edulis) individual collected subtidally; (A, B) are from one colony, (C, D) are from the other; both specimens bleached. (A) Autozooids near colony margin; (B) autozooids in primary layer (large primary orifices), a frontally budded male zooid (small primary orifice, at left), and frontally budded ovicellate zooids; (C) autozooids near colony margin; (D) autozooids in primary layer (large primary orifices), frontally budded male zooids (small primary orifices), and frontally budded ovicellate zooids. Scale bars: 500 Mm.

Figure 13. Porella columbiana O’Donoghue and O’Donoghue, paralectotype, BMNH 1964.1.2.15; bleached: (A) group of autozooids; (B) zooids near colony margin showing stages in formation of suboral avicularian chamber; (C) group of ovicellate zooids; (D) enlargement of autozooidal orifice showing condyles and weak lyrula. Scale bars: 500 Mm (A–C); 200 Mm (D).

Figure 19. (A–D) Microporella neocribroides Dick and Ross: (A) two marginal autozooids; note unusual proximal position of marginal avicularium of zooid at left; (B) enlargement of orifice, ascopore, and marginal avicularium; (C) two ovicellate zooids, each showing a marginal avicularium in typical position; (D) enlargement of ascopore. All specimens bleached. Scale bars: 400 Mm (A); 200 Mm (B); 500 Mm (C); 50 Mm (D).

Figure 20. Microporella ketchikanensis n. sp.: (A) group of marginal zooids with four to five distal spines per zooid; (B) group of marginal zooids with three distal spines per zooid; (C) enlargement of orifice, ascopore, and marginal avicularium; (D) enlargement of proximal orificial margin and ascopore; (E) enlargement of ascopore; (F) group of zooids, two forming ovicells and two with complete, unribbed, umbonate ovicells; note zooid with rare complement of two marginal avicularia. All specimens bleached. Scale bars: 500 Mm (A, B, F); 100 Mm (C); 50 Mm (D); 20 Mm (E).

Figure 22. Fenestrulina delicia Winston, Hayward, and Craig; subtidal specimens from Sitka, Alaska: (A) two complete autozooids and part of an ovicell; lightly bleached for cleaning; (B) group of ovicellate zooids; lightly bleached for cleaning; (C) enlargement of ascopore from zooid at right in Figure 22A above; (D) tatiform ancestrula and periancestrular zooids; unbleached. Scale bars: 500 Mm (A, B, D); 50 Mm (C).

Figure 23. Fenestruloides blaggae Soule, Soule, and Chaney: (A) group of autozooids; (B) enlargement of orifice and ascopore; (C) enlargement of stellate pores and ascopore; note that ascopore has narrower opening than in (B); also note incisions around margin of ascopore depression; (D) two ovicellate zooids; knobs on ovicells are variable, and some ovicells are smooth; (E) marginal zooids, showing pore chambers and stages of ovicell formation; (F) ancestrula (lower centre) and surrounding zooids. All specimens bleached. Scale bars: 500 Mm (A, D–F); 100 Mm (B); 50 Mm (C).

Figure 24. Fenestruloides tongassorum n. sp.; holotype: (A) group of autozooids; (B) enlargement of orifice and ascopore of ovicellate zooid; (C) ovicellate zooids; (D) group of zooids, showing small orifices with closely set distal spines indicative of non-ovicellate zooids, and large orifices with widely set distal spines indicative of zooids that have the potential to form an ovicell. Specimen bleached. Scale bars: 500 Mm (A, C, D); 200 Mm (B).