FLUSTRINA Smitt, 1868

Harmelin, Jean-Georges, 2024, Biodiversity of bathyal coral gardens - portrait of a uniserial bryozoan endemic to the South Azorean Seamount Chain: an unexpected evolutionary testbed?, Zoosystema 46 (30), pp. 749-774 : 751-758

Suborder FLUSTRINA Smitt, 1868

Cribrilina uniserialis Harmelin, 1978: 177 , fig. 2; pl. I, fig. 2.

Harmelinius uniserialis – Rosso in Rosso et al. 2018: 430, figs 85-86.

MATERIAL EXAMINED. — Azores Archipelago. São Miguel Is. • Holotype of Cribrilina uniserialis ; 1 large colony with 1 ovicelled zooid, on Madrepora oculata ; R / V Jean Charcot ; Biaçores Stn 197; 815 m depth; 37°49.5’N, 25°01.5’W; E São Miguel ; 5.XI.1971; MNHN-IB-2008-7908 • Paratype of Cribrilina uniserialis : 1 small colony, on M. oculata ; R / V Jean Charcot, Biaçores Stn 240; 825- 810 m depth; 37°35’N, 25°32.5’W; S of São Miguel Is.; 12.XI.1971; MNHN-IB-2008-7910.

South Azorean Seamount Chain. Atlantis Seamount • Several colonies on M. oculata ; R / V Suroit; Seamount 2; Stn DW 262; 1160 m depth; 34°23.40’N, 30°29.10’W; 3.II.1993; MNHN • 1 colony on Madrepora oculata ; R / V Suroit; Seamount 2; Stn DW 263; 610 m depth; 34°25.90’N, 30°32.50’W; 3.II.1993; MNHN .

Tyro Seamount • Several colonies on Solenosmilia variabilis ; R / V Suroit; Seamount 2; Stn DW 276; 1520 m depth; 34°02.10’N, 28°19.00’W; 6.II.1993; MNHN • Several colonies on M. oculata ; R / V Suroit; Seamount 2; Stn DW 277; 1000- 845 m depth; 33°59.92’N, 28°20.56’W; 6.II.1993; MNHN • Several colonies on M. oculata ; R / V Suroit; Seamount Stn DW 278; 890 m depth; 33°57.80’N, 28°22.40’W; 6.II.1993; MNHN • Several colonies on fragments of M. oculata ; R / V Suroit; Seamount 2; Stn DW 279; 805 m depth; 33°55.60’N, 28°23.70’W; 6.II.1993; MNHN .

Plato Seamount • Small colonies on spines of sea-urchin; R / V Suroit; Seamount 2; Stn DW 248; 670-735 m depth; 33°13.58’N, 29°32.49’W; 1.II.1993; MNHN • 1 colony, on pebble darkened by Mn-Fe oxides; R / V Suroit; Seamount 2; Stn DW 251; 900-935 m depth; 33°13.47’N, 29°38.39’W; 1.II.1993; MNHN .

Irving Seamount • Several colonies on fragments of M. oculata ; R / V Suroit, Seamount 2, Stn DW 221; 1160-1180 m depth; 32°17.84’N, 28°15.32’W; 28.I.1993; MNHN • Several colonies on fragments of M. oculata ; R / V Suroit, Seamount 2; Stn DW 223; 995 m depth; 32°19.69’N, 28°16.50’W; 28.I.1993; MNHN • Several colonies on fragments of M. oculata ; R / V Suroit, Seamount 2; Stn DE 227; 695 m depth; 32°07.20’N, 28°08.70’W, 28.I.1993; MNHN • Several colonies on fragments of M. oculata ; R / V Suroit, Seamount 2, Stn DW 231; 745- 740 m depth; 32°01.5’N, 27°24.50’W; 29.I.1993; MNHN .

Hyeres Seamount • 1 colony ( SEM pictures) on stylasterid skeleton; R / V Calypso , survey 1959, 620- 700 m depth, 31°27.7’N, 28°55.6’W; 13.VIII.1959; MNHN • Several colonies on skeleton of M.oculata ; R / V Suroit; Seamount 2; Stn DW 184; 706- 675 m depth; 31°24.40’N, 28°52.3’W; 13.I.1993; MNHN • Several colonies, on skeleton of M. oculata ; R / V Suroit; Seamount 2; Stn DW 200; 1060 m depth; 31°19.10’N, 28°36.00’W; 18.I.1993; MNHN • 1 colony, on skeleton of M. oculata ; R / V Suroit; Seamount 2; Stn DW 203; 845 m depth; 31°09.50’N, 28°43.50’W; 19.I.1993; MNHN .

Great Meteor Bank • 1 fragmented colony, on rock fragment darkened by Mn-Fe oxides; RV Suroit; Seamount 2; Stn DW 180; 1575-1610 m depth; 30°04.09’N, 28°45.09’W; 15.I.1993; MNHN .

AMENDED DESCRIPTION

Colony encrusting, fundamentally uniserial, consisting of a primary linear chain formed by distally budded caudate autozooids and kenozooids, from which secondary ramifications are bilaterally budded ( Fig. 2 C-E), their development possibly leading to the spotty formation of reticulate or pseudo-pluriserial subcolonies ( Fig. 3C, E ). Reticulate structure formed in three ways: 1) intersecting of two overlapping branches; 2) real connection of two branches via their communication pores; and 3) distal zooid of a branch abutted onto the lateral side of another branch ( Figs 3A ; 8C ). Small pseudo-pluriserial subcolonies can develop by disordered aggregation of autozooids with reduced cauda and kenozooids, both being more or less interconnected.

Autozooids with a cormidial structure, typically with a proximal cauda budded by the parent zooid, widening distally to form the autozooidal chamber with gymnocystal lateral walls and a costate shield and, distally to the orifice

and fully integrated to it, a distal kenozooid forming a cap from which is budded a daughter autozooid or a vicarious kenozooid. Caudae semi-cylindrical, long (200-400 µm) and narrow or much shorter (40 µm) or nearly absent, with a smooth gymnocystal wall through which a tubular coelomic lumen is visible, broadening distally to become the proximal part of the main chamber. Main chamber with lateral walls with a greater or lesser degree of slope, bearing one to three elongated pore chambers on each side, a costate frontal shield made of 14-21 costae ( Table 1 ). Costae with upper surface rounded, smooth and without pelmatidia (lumen pores), separated on each side by a slit without intercostal bridges, generally narrow but occasionally much wider; paired costae sometimes of different width, fused in the midline and forming a low, irregular bulge; distalmost pair of costae playing the role of an apertural bar, similar to the proximal ones but wider (60-80 µm vs 35-50 µm), sometimes forming an obtuse angle; costae of the proximal corner of the costate shield much smaller than the others. Orifice large, terminal, laterally and distally delimited by a semicircular calcified frame, sometimes very thick and made of multiple calcified layers produced by intramural budding (see below), proximally edged by the distalmost pair of costae; operculum with a sightly convex proximal edge. Oral spines absent. Distal kenozooid prolonging the autozooidal chamber below the level of the orifice, in the shape of the upper half of a truncated cone (“kenozooidal cap”) at the top of which is budded a distal daughter zooid ( Fig. 4 AD), its chamber connected to the maternal autozooid by a foramen, i.e., a large, circular pore (18-25 µm in diameter) open through the transverse wall ( Figs 4A, B ; 9E ), assumed to function as a gigantic pore chamber.

Ovicelled zooids very infrequent (<1.5% of autozooids, Fig. 3A ), often grouped, with costate shield, apertural bar and orifice broader than in non-ovicelled zooids ( Table 1 ). Ovicell prominent, apparently cleithral ( Fig. 5 ); brood chamber budded from the transverse wall of the maternal autozooid ( Fig. 5C, D ); ooecium bilobed with a frontal medial suture, produced by a basal ooecial kenozooid with a frontally apparent distal part from which is budded a distal zooid ( Fig. 5A, B ). Ooecial kenozooid communicating with the maternal autozooid by a foramen ( Fig. 5C, D ) identical to that connecting a non-ovicelled autozooid to its distal cap; basal part with a pore-chamber on each side, producing a bilobate outfold with a smooth surface without pores, a thick (20 µm), alveolar wall (ectooecium), which is proximally and basally divided in two sheets forming each lobe ( Fig. 5D ). Medial suture of the two lobes closed or partially open with an elongated distal window reaching the distal edge of the ovicell ( Fig. 5A, B ). Distal, frontally apparent part of the ooecial kenozooid ( Fig. 5A, C, D ) larger than the distal cap of non-ovicelled zooids, with a frontal, circular window open near the distal edge of the medial suture, similar to that present on vicarious kenozooids (see below), opening on a thick, multi-layered wall and a small central opesia; porous knobs (see below) present near this window ( Fig. 5A, B ).

Avicularia displaying a variety of shapes assigned to five different morphs (AV 1-5), budded by autozooids (AV 1-5) or vicarious kenozooids (AV 4 & 5) ( Figs 6 ; 8 ). All avicularian morphs with semicircular rostrum and mandible, not prominent, operculum and opesia rounded with a narrow cryptocyst, no pivot bar or hinges, and two large basal pores; present on all ovicelled autozooids, less frequently present on non-ovicelled zooids ( Table 2 ).

AV1: “columnar” ( Figs 6B ; 8D ), with a slightly barrel-shaped column, two large basal pores in opposite position on the proximal and distal sides, infrequent, adventitious on ovicelled and non-ovicelled autozooids, single or paired, budded on the vertical wall between the apertural bar or the preceding costa, uncalcified area oval, with semicircular opesia a little broader than the mandible, a narrow rim of cryptocyst slightly broader proximally.

AV2: “globular” ( Figs 6G, H ; 8E ), similar to AV1 but shorter and rostrum with a wider, rounded rim, adventitious on ovicelled and non-ovicelled autozooids

AV3: “adnate” ( Figs 6A, D ; 8A ), with a triangular silhouette, adventitious on ovicelled zooids, two large basal pores in opposite position similar to those of AV1, occurrence of peripheral porous knobs ( Figs 6D ; 8A ).

AV4: “pyramidal” ( Figs 6E, G ; 8B ), with a broad base partly resting on the substratum, column sculpted by vertical grooves, single, sometimes paired with AV2 when distolaterally budded by a non-ovicelled zooid ( Fig. 6G ), or several, up to five, laterally budded from both sides of an autozooid ( Fig. 6E ), occasionally budded by a vicarious kenozooid ( Fig. 6H ); presence of 2-3 porous knobs ( Fig. 8B ).

AV5: “giant” ( Figs 6C, H ; 8C ), rare (only two cases observed), laterally budded by a vicarious kenozooid ( Fig. 6H ) or a non-ovicelled autozooid; chamber very large, slightly convex, roughly pentagonal with a broad base resting on the substratum, adjoining the parental zooid with wrinkles at the budding locus, a pair of lateral pore chambers; mandible and opesia area centrally located, both similarly semicircular, the rostrum a little smaller and edged by a low rim; occurrence of porous knobs (see below), one distal to the rostrum and four around the opesia ( Figs 6C ; 8C ).

Vicarious kenozooids (“vicariozooids”, Silèn 1977; Schack et al. 2019) frequent (mean: 21% up to 56% on a pebble from DW251; Fig. 3E ), produced by distal or lateral budding from an autozooid or a kenozooid, irregularly shaped and sized ( Figs 3A, 3D ; 9 A-F; 10A; Table 1 ), often as large as an autozooid, sometimes larger or much smaller, polygonal with rounded corners, eventually with a short conical cauda when included in a zooid chain, proximal base upwardly protruding on the wall of the parental zooid when laterally budded ( Figs 3A ; 9D, E ); distal edge very wide and rectilinear when abutting on to the lateral side of an autozooid ( Figs 3A ; 8C, D ). Calcified frontal wall a smooth, convex gymnocyst, entirely covered by a thick, persistent cuticule (6F, H) with a pair of fusiform pore chambers placed at half height on each lateral side and a large central window (90-110 µm) oval to circular, opening onto the thick, stratified gymnocystal wall ( Fig. 9 D-F), the innermost layer, a smooth cryptocystal rim surrounding a small, rounded opesia (diameter: 30-40 µm) opening on a large, irregularly shaped coelomic chamber visible by light microscopy ( Fig. 8A, B ), with lateral tubular extensions connected to adjacent zooids, whose assumed function is to ensure the continuity of the funicular system. Presence on the frontal wall, close to the central window, of several (up to 7) short porous knobs (diameter: 8-11 µm) with open tips ( Figs 8E, F ). Secondary kenozooids eventually produced by intramural budding within the cystid of a damaged or senescent autozooid (see below).

Ancestrula rare, similar to non-ovicelled autozooids but considerably smaller ( Fig. 4E ); orifice relatively large, costate frontal shield composed of 14 costae, with a broad apertural bar; distal cap small. Zone of astogenetic change consisting of a uniserial file of daughter zooids similar in shape and size to the ancestrula, produced by the latter from a distal or a proximal budding locus ( Fig. 4E ).

Figures

FIG. 2. — Harmelinius uniserialis (Harmelin,1978),colonized substrates and general aspect of colonies:A, fragment of Madrepora oculata Linnaeus,1758;B, pebble; C, part of colony showing non-caudate autozooids, optical view; D, other aspect of the same colony, SEM view; E, part of colony with typical features. Origin: A, C, D, Hyères SMT, Stn DW 184; B, Irving SMT, Stn DW 251; E, Tyro SMT, Stn DW 276. Scale bars: A, B, 1 cm; C, D, 1 mm; E, 400 µm.

FIG. 3. — Harmelinius uniserialis (Harmelin,1978),structure of colonies and graphs of zooid proportions:A - a, distal budding of autozooids with long cauda;b, lateral budding of autozooid (AZ) and kenozooid (KZ); c, abutment of kenozooid on ovicelled AZ - 1, KZ (21% white),non-ovicelled AZ (78% grey),ovicelled AZ (1% black); 2, non ovicelled AZ without avicularium (AV) (59% white), with one AV (24% grey), with two AV (17% dark); 3, ovicelled AZ, with one AV (23% grey), with two AV (77% dark);B, ovicellar kenozooid connected to the lateral pore chamber of an adjacent AZ; C, zooidal aggregation with 12 AZ without cauda, 28 AV and three KZ;D, clustering of three AZ without cauda,involving a small vicarious kenozooid abutted on to an avicularium (AV4) in proximal position,co-occurring with another AV type (AV2); E, dense aggregation of KZ. Origin:A, B, Tyro SMT,Stn DW 276;C, D, E, Tyro SMT,Stn DW 278.Scale bars: A,C, E, 400 µm;B, D, 200 µm.

FIG. 8. — Harmelinius uniserialis (Harmelin, 1978), drawings of five types of avicularia: A, “adnate” (AV3); B, “pyramidal” (AV4); C, “giant” (AV5); D, “columnar” (AV1); E, “globular” (AV2). Origin: copied from diverse SEM pictures. Scale bar: 50 µm.

FIG. 4. — Harmelinius uniserialis (Harmelin, 1978), morphology of non ovicelled autozooids and ancestrula: A, autozooid (AZ) with two avicularia (AV1) and distal budding from the kenozooidal cap, budded from the lateral side of another AZ; B, AZ distal part with a AV1 avicularium, note the foramen through the transverse wall separating the AZ orifice from the kenozooidal cap (idem in A), the concave proximal edge of the orifice and the unequal size of costae; C, eroded kenozooidal cap showing its subconical chamber and the broken base of the AZ transverse wall; D, distal part of AZ showing the boundary between the kenozooidal cap and the orifice frame; E, ancestrula and AZ, note their contrasting sizes and the proximal budding by the ancestrula. Origin: A, B, C, Hyères SMT, Stn DW 200; D, E, Tyro SMT, Stn DW 276. Scale bars: A, B, E, 200 µm; C, D, 100 m.

FIG. 9. — Harmelinius uniserialis (Harmelin, 1978), vicarious kenozooids: A, drawing of two interconnected KZ, laterally budded by 2 AZ; B, light photography of the same zooids; C, part of colony with seven variously shaped KZ connected to several AZ; D, two differently sized KZ budded from the lateral walls of two AZ; E, pentagonal KZ with proximal corner folded on the budding locus of the maternal zooid; F, frontal wall of a large KZ with central window open on a thick, multilayered wall, surrounded by seven porous knobs. Distansescharella d’Orbigny, 1853: G, D. alcicornis (Jullien, 1882), large vicarious KZ with central window, abutted on to an AZ and close to an adventitious avicularium; H, D. seguenzai Cipolla,1921, reticulum formed by three small KZ with a central window surrounded by 2-5 conical spinous processes with a likely porous tip; I, D. alcicornis, avicularium with opesia and rostrum poorly differentiated, and proximal side folded on the maternal zooid. Origin: A, B, Azores, São Miguel bathyal slope, Biaçores Stn 197, 815 m (9A copied from Harmelin 1978, fig. 2); C, F, Hyères SMT, Stn DW 200; D, E, Tyro SMT, Stn DW 276; G, I, R/V Thalassa, Y434,620 m, on Lophelia prolifera (Linnaeus, 1758); H, R/V Calypso, Stn 1902, Libya. Scale bars: A, B, D, F, 200 µm; C, 400 µm; E, G, H, 100 µm; I, 50 µm.

FIG. 5. — Harmelinius uniserialis (Harmelin, 1978), structure of the ovicell: A, distal part of an ovicelled autozooid bearing two adnate avicularia (AV3), with open medial slit, and ooecial kenozooid budding a distal zooid; B, close-up of the same ovicell, medial slit showing the two layers of the bivalved ooecial wall, the dorsal window of the distal kenozooid with thick gymnocystal layers and oval opesia, and two lateral porous knobs; C, ovicell in formation showing the floor of the brood chamber budded by the maternal autozooid; D, broken ovicell showing the thickness of the frontal wall and the two proximal layers, and the foramen open through the transverse wall. Origin: A, B, C, Tyro SMT, Stn DW 276; D, Hyères SMT, Stn DW 184. Scale bars: A, C, D, 100 µm; B, 50 µm.

FIG. 6. — Harmelinius uniserialis (Harmelin, 1978), different types of avicularia: A, “adnate” type (AV3) on an ovicelled AZ; B, “columnar” type (AV1); C, “giant” type (AV5) with three porous knobs, one incompletely formed, distal to the slightly prominent rostrum; D, “adnate” type, adventitious to an ovicelled AZ, with a large pore chamber and three porous knobs (inset: enlarged view of a knob); E, autozooid with five “pyramidal” morphs (AV4) budded from lateral walls; F, vicarious kenozooid with thickened cuticule persisting on the frontal gymnocyst and the central window; G, globular and pyramidal avicularia budded by the same AZ; H, three globular (AV2), one “giant” (AV5) and one “pyramidal” (AV4) avicularia budded by two AZ and a vicarious KZ with persistent cuticular layer; Origin: A, D, Tyro SMT, Stn DW 276; B, Hyères SMT, Stn DW 200; C, E, F, G, H, Tyro SMT, Stn DW 278. Scale bars: B, C, D, 50 µm; A, F, G, 100 µm; D, H, 200 µm.