Erect bifoliate species of Microporella (Bryozoa, Cheilostomata), fossil and modern

Microporella Hincks, 1877 is one of the most diverse genera of cheilostome bryozoans, containing more than 150 named species. Distributed globally since the early Miocene, the majority of species of Microporella have sheet-like colonies encrusting hard and / or ephemeral substrates, while a limited number of species have erect bifoliate colonies starting from an encrusting base. Herein, the four nominal species of erect bifoliate Microporella (M. bifoliata, M. hastigera, M. hyadesi and M. ordo) are revised, and one new Pliocene (M. tanyae sp. nov.) and three new Recent species (M. ordoides sp. nov., M. lingulata sp. nov. and M. modesta sp. nov.) are formally described. Furthermore, the lectotype and paralectotypes were designated for M. bifoliata and M. hastigera. An additional Recent species, Microporella sp. 1, is also described and illustrated but left in open nomenclature owing to the absence of ovicells in the single available fragment. Although the molecular phylogeny of Microporella has yet to be resolved, the diversity of character states present among the erect bifoliate species described here suggests that this colony growth-form is not monophyletic but has evolved on multiple occasions.


Introduction
Ascopore field. A narrow, raised area of gymnocystal calcification beneath level of adjacent frontal shield but at approximately same level as orifice, located very close to its hingeline; elliptical, ca 35 × 50 µm, distal margin with projecting, semielliptical tongue leaving a crescent-shaped opening, ca 10 × 30 µm, with radial spines.
Avicularium. Single, located at the same level of ascopore, oriented laterally; crossbar complete; opesia semielliptical; rostrum subtriangular, the distal end a little rounded, not channelled. Ovicell. Prominent, circular in outline, not personate and not obscuring orifice; calcification similar to frontal shield; pseudopores variable in number, scattered over entire surface, variably spaced.
The form of the mandible is not known in this fossil species, but the fact that the avicularia have closed distal ends without channels may suggest that mandibles were not setose and had a shape identical to that of the rostrum.

Etymology
Named after Dr Tanya Knowles who collected the specimens in 2006.

Description
Colony. Starting with an encrusting unilaminar and multiserial base, later becoming erect with bifoliate fronds up to several cm wide; interzooidal communication not observed.
Autozooids. Distinct, separated by narrow grooves, rhomboidal, longer than wide (mean L / W = 1.39). Frontal shield moderately convex, finely and densely granular; marginal areolae typically numbering about 10 (8-12), variable in size (15-60 µm), funnel-shaped, sometimes subdivided internally; up to about eight non-marginal pseudopores, morphologically very similar to areolar pores, generally placed more centrally on the frontal shield at the same level as the avicularium or slightly below, irregularly spaced, sometimes internally subdivided.
Ascopore field. A narrow, raised area of gymnocystal calcification beneath level of adjacent frontal shield but at approximately same level as orifice, located very close to its hingeline; elliptical, ca 30- Avicularium. Single, located between level of ascopore and lateral corner of rhomboidal autozooid, oriented laterally to slightly distolaterally; crossbar complete; opesia semielliptical; rostrum subtriangular, channelled.

Remarks
This extinct species was found in the Pliocene of Virginia. Although very similar to the Miocene Microporella bifoliata, the new Pliocene species shows slightly shorter but wider, and consequently squatter, autozooids with larger orifices, larger avicularia and broader ovicells. Additionally, the rostrum in M. tanyae sp. nov. narrows distinctly immediately distal to the crossbar, which does not seem to be the case in M. bifoliata specimens, and the orifice seems to be more clearly D-shaped with the proximal margin somewhat straighter.

Description
Colony. With an encrusting unilaminar and multiserial base, later becoming erect bilaminar, robust branching (adeoniform); branches narrow, 2-3 mm wide with usually 4-5 but up to eight linear series of alternating zooids on each side; interzooidal communication via multiporous septula.
Autozooids. Rhomboidal to hexagonal, longer than wide (mean L / W = 1.21). Frontal shield relatively flat to moderately convex, entirely covered by distinct nodules of varying shape with 30-35 pseudopores (diameter 5-15 µm) intercalated between them, plus 5-10 round marginal areolar pores, larger than frontal pores (diameter 20-45 µm); except for a single areolar pore distal to avicularium rostrum, area between proximal margin of the orifice and ascopore field and directly proximally to avicularium rostrum usually devoid of pores.
Primary orifice. Transversely D-shaped with a straight, distinctly crenulated hingeline; in each corner a short, blunt denticle directed distally; distolateral orificial rim with numerous low rounded and irregularly distributed denticles of variable size; operculum smooth but with a broad and slightly bent transverse depression in the centre; three or four distal oral spines (diameter 15-20 µm); no peristome. Ascopore field. Outlined by a low rim and a narrow, raised band of gymnocystal calcification, located at ca 65 µm from hingeline of the orifice, slightly displaced to the side by the avicularium and often obliquely aligned; gymnocystal field elliptical, ca 50-60 × 70-80 µm; distal margin with median, subrectangular, projecting tongue leaving a C-shaped opening, ca 10 × 50 µm, delimited by finely spinose margins.
Avicularium. Single, placed in close proximity of and lateral or proximolateral to ascopore; rostrum directed distolaterally, broadly triangular with an open funnelled tip and thin raised lateral margins,  slightly acute to frontal plane; mandible lanceolate, significantly exceeding length of rostrum, ca 230 µm long, abruptly decreasing in width between crossbar and rostrum and slightly widening distal to rostrum before thinning again, the distal third or quarter very narrow and downcurved; proximal and distal opesia semicircular, divided by a straight and thin but deep crossbar.
Ovicells. Globular, entirely obscuring the orifice; surface densely nodular and with numerous pseudopores seemingly aligned in radial rows, the proximolateral margins joining the proximolateral orifice corners, opening arched above proximal orifice margin, often equipped with a slightly projecting lip.

Remarks
This species was originally recorded from off western and northern Pico Island (Azores, central Atlantic) from depths between 80 and 820 m. During the French Biaçores expedition it was also  (d'Hondt 1975). Previous records of this species, especially those pre-dating the advent of scanning electron microscopy (e.g., Calvet (1931) from Cape Verde Islands at 52 m depth), need to be revised. (Jullien, 1888) Fig. 6;  Autozooids. Rounded rectangular to hexagonal, longer than wide (mean L / W = 1.67), distinct with interzooidal boundaries marked by thin band of slightly raised calcification on either side of a narrow groove. Frontal shield flat to very slightly convex, pustulose; marginal areolar pores numbering about 10, elongate near growing edge, becoming smaller, equidimensional and almost indistinguishable from pseudopores, except for those at the proximolateral corners of the zooid which remain larger (diameter 20-40 µm); pseudopores numerous (about 50), small (diameter 5-15 µm), irregularly scattered among pustules.
Avicularium. Single, moderately large, present in the majority of autozooids, sometimes lacking in smaller zooids, especially immediately following row bifurcations; positioned level with the ascopore, oriented distolaterally, usually at about 60° to the long axis of the autozooid; crossbar calcified; opesia semielliptical; rostrum short, broadly subtriangular with concave sides, the distal end rounded, distinct channel present. Mandible in dried material narrow, short (ca 50-65 µm) and pointed triangular.
Ovicells. Very large, sometimes covering frontal shield of distal zooid as far as ascopore, bulbous, usually a little longer than wide, personate or semi-personate with variably-developed lobes extending proximally of orifice, calcification fabric similar to frontal shield but with finer pustulation, smoothly continuous with frontal shield of distal zooid; small pores scattered over entire surface, denser close to lateral and distal margins; secondary orifice of personate ovicellate zooids of reduced length, typically boat-shaped, the distal edge concave, the proximal edge convex.

Remarks
This species has been recorded from the subantarctic, Cape Horn and Tierra del Fuego. Records from the Indian Ocean (Thornely 1912) and New Zealand (Brown 1952;Powell 1967) are probably misidentifications, the latter possibly M. ordo (see Di Martino et al. 2017: fig. 6). It is very common in material from several widely dispersed Discovery Stations from depths of 49 to 341 m in the South Atlantic around Cape Horn, the Falkland Islands, Burdwood Bank, the southern Patagonian Shelf, Shag Rocks and South Georgia (Hayward & Ryland 1990). Many of the colonies show extensive circular boreholes, about 0.12 mm in diameter, which penetrate autozooidal frontal shields and ovicells ( Fig. 6C-D). Similar boreholes were interpreted by Wilson & Taylor (2006) as evidence of boring predation.

Description
Colony. Erect, bifoliate, the largest about 110 × 75 mm, with broad branches fused at edges to form a boxwork colony; interzooidal communication via multiporous septula, elliptical, 55 µm long by 45 µm wide, with at least 12 circular pores ca 4 µm in diameter, placed in the basal lateral walls on distolateral corners of autozooids.
Orifice. Semielliptical, significantly wider than long, hingeline straight to weakly concave, with about 15 teeth, equal in size except for slightly longer outer one or two pairs; oral spines lacking; folded back transverse vertical wall of distal zooid forming a slightly elevated crescent secondary rim above the distal margin of the primary orifice; operculum smooth.
Ascopore field. As a raised area of gymnocystal calcification at approximately same level as orifice but beneath level of adjacent frontal shield, located moderately close to orifice hingeline, about 60-70 µm below, separated from it by non-porous pustulose cryptocyst; reniform to transversely elliptical, 45 × 60 µm, opening heart-shaped, 25 × 40 µm, covered by filigree sieve plate, a narrow, bifurcated tongue usually projecting from the distal edge.
Avicularium. Single, moderately large, present in the majority of autozooids, positioned level with or slightly distally of and almost abutting the ascopore, oriented distolaterally to almost laterally; crossbar complete; opesia semielliptical; rostrum short, teat-shaped, the distal end rounded, distinct channel present. Mandible in dried material with short (ca 90-110 µm) pointed seta, narrow throughout, hooked on underside, lying across or a little proximal of ascopore when open.
Ovicells. Very large, often covering frontal shield of distal zooid as far as ascopore, bulbous, subcircular or a little longer than wide, non-personate; calcification similar to frontal shield but with finer pustules, continuous with frontal shield of distal zooid; small pseudopores distributed across entire surface, more closely spaced compared to those on the frontal shield, radially aligned near margins; orifice of ovicellate zooids hidden in frontal view.

Remarks
The description given above and measurements in Table 5 are based on Recent examples of this species which show the morphology of the species better than the type and other fossil material. Although very similar to Microporella hyadesi in its general appearance, M. ordo is easily distinguished by its heartshaped ascopore with filigree sieve plate and narrow bifurcated tongue, in addition to the non-personate ovicells.
The present-day range of the species extends from NW of the Three Kings Islands at Middlesex Bank to Ranfurly Banks off East Cape, New Zealand (33.9-37.6° S; depth 46-96 m).    Table 6 Diagnosis Colony erect, bifoliate; branches narrow. Autozooids rhomboidal. Frontal shield pustulose, pseudoporous. Orifice semielliptical; hingeline with equal-sized teeth, the outermost smaller; oral spines lacking. Ascopore subcircular, opening horseshoe-shaped covered by a filigree sieve plate and a narrow tongue projecting from the distal edge. Avicularium single, placed level with ascopore, oriented distolaterally; crossbar complete; opesia semielliptical; rostrum channeled. Ovicells personate or semipersonate.

Etymology
Referring to its similarity with Microporella ordo Brown, 1952.

Description
Colony. Erect, bifoliate; the longest colony observed about 54 mm with the broadest frond about 15 mm, consisting of more than 30 linear series of alternating zooids; growing edge stepped; interzooidal communications not observed.
Orifice. Semielliptical, significantly wider than long, hingeline straight or somewhat convex, with about 17 teeth, equal-sized apart from the outermost few which are smaller; oral spines lacking; folded back transverse vertical wall of distal zooid forming a crescent above the distal part of the primary orifice.
Ascopore field. As a raised area of gymnocystal calcification at approximately same level as orifice but beneath level of adjacent frontal shield, located moderately close to orifice hingeline, about 60-70 µm below, separated from it by non-porous cryptocyst with smaller than average pustules; subcircular, 45-60 µm in diameter, opening horseshoe-shaped, 10-15 × 30-35 µm, covered by filigree sieve plate, a narrow, straight tongue usually projecting from the distal edge.
Avicularium. Single, moderately large, present in the majority of autozooids; positioned level with or slightly proximally of ascopore, oriented distolaterally; crossbar complete; opesia semielliptical; rostrum short, teat-shaped, the distal end rounded, distinct channel present. Mandible 160-180 µm long, narrow and pointed. Ovicells. Large, bulbous, subglobular or a little longer than wide, personate or semipersonate, proximal arms forming bridge above ascopore; calcification of similar fabric to frontal calcification, continuous with frontal shield of distal zooid; pores small, sparse, mostly located near margins; partly formed ovicells common; orifice of ovicellate zooids hidden in frontal view; secondary orifice of personate ovicells boat-shaped with convex proximal and concave distal edge.

Remarks
This new species is extremely similar to Microporella ordo but differs in a sufficiently large number of characters to justify recognition as a separate species. Colonies of M. ordoides sp. nov. have narrow branches, contrasting with the broad fronds of M. ordo, and the growing edge is stepped rather than smooth. Differences in zooidal morphology include the greater number of pseudopores in the frontal shield of M. ordoides sp. nov., smaller outer teeth on the hingeline of the orifice, a horseshoe-shaped ascopore opening, personate or semi-personate ovicells containing fewer pores, and avicularia tending to be located more proximally than in M. ordo. Specimens of M. ordoides sp. nov. were collected off Campbell Island (New Zealand) on the Campbell Plateau at a depth of 159-435 m.

Etymology
From the Latin ʻlingulataʼ, meaning tongue-shaped and referring to the shape of the colonies.   . 9).

Description
Colony. Erect, bifoliate, comprising a single, non-bifurcating branch, tongue-shaped, 4-6 mm long by 3-4 mm wide (0.5-1 mm at the tip), proximal end rounded, distal end truncate forming growing edge; basally unattached; interzooidal communications not observed. Apparent ancestrula ascophoran in morphology (damaged in scanned examples), about 300 × 185 µm, with an associated avicularium; located on one side of branch close to but not at proximal extremity of colony, oriented proximally. New buds at distal growing edge oriented obliquely to colony axis, facing distolaterally to the left on the left side and distolaterally to the right on the right side; zig-zag seam between left-and right-facing zooids approximately parallel to axis but typically displaced from midline.
Avicularium. Single, moderately large, present in most autozooids, located on right of autozooids at the left side of colony and on the left of those at the right side; level with or distal of ascopore, oriented laterally or slightly disto-laterally; crossbar deep, distal edge straight, proximal edge scalloped; opesia semielliptical; rostrum short, subtriangular, the distal end rounded and without a channel. Mandible long, ca 315-450 µm, lanceolate, pointed, slightly hooked, open examples mostly lying across ascopore. Intramural budding common in avicularia.
Ovicells. Large, low in profile, not personate; calcification of identical fabric to frontal shield, continuous with frontal shield of distal zooid; pores irregularly scattered over surface; secondary orifice of ovicellate zooids shallower than infertile zooids.

Remarks
The ascopore of this new species is unusually wide compared with congeners, and the flat-topped cryptocystal pustules are another very notable feature. However, it is the peculiar tongue-shape of colonies that provides the easiest way of recognizing Microporella lingulata sp. nov. while at the same time posing questions about its mode of life. No substrate of attachment is visible, although it is possible  that a small substrate is present but totally enveloped by later growth. Regardless, it is difficult to understand how adult colonies were supported as there are no indications of rhizoids to root the colonies into a particulate substratum, nor are rhizoids known in any other species of Microporella. Functional autozooids were evidently budded at equal rates on both sides of the branch, arguing against the idea that colonies rested horizontally on the sea-bed with one side down against the sediment. The most plausible options are either a vertical orientation with only the rounded proximal end embedded in the sediment, or the entire colony living interstitially within a coarse substratum. According to St. B263 sediment data, the seafloor at the exact locality that yielded the specimens comprises medium and fine sand (62.5 to 500 µm particle size). Given the colonies are not rooted, it is possible that they just sit on the seafloor. The robust avicularian mandibles may have a supportive role, perhaps analogous to that in free-living lunulitiform bryozoans (e.g., Chimonides & Cook 1981).

Etymology
From the Latin ʻmodestaʼ, meaning modest, moderate and referring to the ascopore concealed beneath a mucro.

Description
Colony. Erect, bifoliate, branches narrow, strap-like, ca 5 mm wide with up to 15 linear series of alternating zooids on each side; growing edge stepped; interzooidal communications not observed.
Orifice. Transversely D-shaped, over twice as wide as long, hingeline straight or slightly concave, equipped with a large tooth close to each end and numerous tiny teeth in between; low cowl-like peristome sometimes developed distally around orifice; three or four oral spines (diameter 10-15 µm), a spine just above each proximolateral corner of orifice plus a single distal median spine or spines inwards of the two distolateral corners.
Ovicells. Moderately large, subglobular or rounded quadrate, not personate, proximal arms forming bridge above ascopore; calcification of similar fabric to cryptocyst but pustules smaller and more closely-spaced, continuous with frontal shield of distal zooid; pseudopores small, peripheral only, those near margins aligned in radial rows; orifice of ovicellate zooids partly hidden in frontal view.

Remarks
This is the only bifoliate species of Microporella known from the Mediterranean (coast of Algeria). The presence of a mucro projecting over the ascopore enables M. modesta sp. nov. to be readily distinguished from its bifoliate congeners described above, as well as the encrusting European species of Microporella (i.e., M. ciliata (Pallas, 1766), M. marsupiata (Busk, 1860), M. appendiculata (Heller, 1867)). The

Description
Colony. Erect, bifoliate, branches narrow; fragment available ca 3 mm wide with up to six linear series of alternating zooids on each side; interzooidal communications through multiporous septula visible at colony growing edge.
Ascopore field. As a narrow band of gymnocystal calcification, at approximately same level as orifice but beneath level of adjacent frontal shield, located at ca 55-75 µm from the orifice hingeline, separated from it by non-porous pustulose cryptocyst; circular (diameter 50-60 µm) to transversely elliptical (55 µm long by 80 µm wide), opening C-shaped, 10 × 50 µm, with tiny radial denticles, and a circular tongue projecting from the distal edge.
Avicularium. Usually single, rarely paired, moderately large, present in all autozooids, positioned at level with the ascopore, oriented distolaterally, usually at about 45° to the long axis of the supportive autozooid; crossbar calcified; opesia semielliptical; rostrum short, subtriangular with concave sides, the distal end rounded, distinct channel present. Mandible 150-180 µm long, narrow and pointed. Multiple intramural buds observed in avicularia.

Remarks
Among all bifoliate congeners, Microporella sp. 1 mostly resembles M. hyadesi. The two species share a transversely D-shaped orifice with equal-sized teeth in the hingeline, the characters of the ascopore and the appearance of the frontal shield made of flat-topped pustules. Differences include: the shape of the zooids (mean L / W = 1.67 and 1.31, respectively) which are rectangular and flat in M. hyadesi, rhomboidal to hexagonal and convex in Microporella sp. 1; the avicularium is more laterally oriented and has a wider channel in the rostrum than M. hyadesi. The two species also differ in their geographical distributions. The single available fragment of Microporella sp. 1 was found at Puysegur Bank, south west of South Island of New Zealand at a depth of 187 m, while M. hyadesi is a South Atlantic species found at a depth of 49-341 m (Hayward & Ryland 1990).    (Fig. 13). Among these, only M. ordo was first described from Pleistocene deposits in the Wanganui Basin, New Zealand.
Two other genera of Microporellidae -Diporula and Flustramorpha Gray, 1872 -comprise Microporella-like species having erect colonies with cylindrical and bifoliate branches, respectively. However, colony growth-form alone seems a feeble character to justify the distinction among the three genera. In fact, most erect bilaminate colonies start with a more or less developed encrusting base before growing as erect bilaminate sheets back-to-back. For example, Microporella tanyae sp. nov. starts with an extended encrusting base completely wrapping the shelly substrate (see Fig. 2). In addition to the colony growth-form, Hincks (1880: 220) emphasized the different structure of the orifice, semicircular in Microporella, horseshoe-shaped in Diporula. The shape of the orifice may also be somehow variable.
In encrusting species of Microporella from Hokkaido (Japan), the shape of the orifice varies from higharched semicircular to transversely D-shaped, to oval (Suwa & Mawatari 1998).
The diagnosis of the genus Microporella given by Hayward & Ryland (1999: 292) includes an imperforate ooecium and the presence of conspicuous basal pore-chambers, while in the diagnosis of Diporula (Hayward & Ryland 1999: 302) the ooecium is perforate and basal pore-chambers are substituted by small multiporous septula. However, pseudopores also occur in the ooecium of many encrusting species of Microporella, including the type species Microporella ciliata (see Kukliński & Taylor 2008: fig. 1c).
The presence of small multiporous mural septula in lateral walls has been also observed in erect bifoliate species of Microporella (e.g., Microporella ordo, Fig. 7D).
Microporella hastigera offers an example of how the boundaries among Microporella, Diporula and Flustramorpha can be indistinct. Busk (1884: 135), who originally described Microporella hastigera as Flustramorpha, expressed his doubts about the separation of this genus from Microporella based solely on colony growth-form, and suggested that Flustramorpha may be a subgenus of Microporella. Subsequently, M. hastigera was placed in Diporula and eventually in Microporella by Calvet (1931) andd'Hondt (1975), who regarded Diporula as a synonym of Microporella.
A meaningful phylogenetic analysis of Microporella and closely-related genera (i.e., Diporula and Flustramorpha) currently in progress will be of paramount importance to resolve the phylogenetic relationships of microporellids and offer robust evidence for formal synonymy of these genera.