Fenestrulina malusii (Audouin & Savigny, 1826)

Rosso, Antonietta, Di Martino, Emanuela, Donato, Gemma, Figuerola, Blanca, Gerovasileiou, Vasilis, Siddiolo, Chiara, Sinagra, Alessandro, Sanfilippo, Rossana & Sciuto, Francesco, 2025, Unlocking Mediterranean bryozoan diversity: seven new species unveiled after fixing a neotype for Fenestrulina malusii (Audouin & Savigny, 1826) (Cheilostomatida, Fenestrulinidae), ZooKeys 1254, pp. 1-74 : 1-74

Fenestrulina malusii (Audouin & Savigny, 1826)

Figs 1 , 3 , 4 , 5 , 6 , 22 , 23 , 24 ; Tables 1 , 2

Fenestrulina malusii Audouin 1826: 239, pl. 8, fig. 8.

Fenestrulina malusii Audouin : Di Geronimo et al. 1988; 1990: table 1; Rosso 1989: tables 3 d, 4 d.

Type material.

Italy • Neotype 1 ovicellate colony, including the regenerated ancestrula and more than 100 autozooids. On fronds of Laminaria rodriguezii Bornet , Mediterranean, Tyrrhenian Sea, southwest of Ustica Island, Apollo Bank ; 38°7'N, 13°1'E; 60 m depth; Jun. 1986; I. Di Geronimo leg.; scuba diving; PMC.B 37. Neotype 23.2.2024 .

Other examined material.

Italy • 18 small colonies, each including tens of autozooids, with ancestrula and ovicells, except for one only consisting of a large lobe of ~ 30 autozooids; same details as the neotype; PMC Rosso-Collection I.H.B.115.a . Italy • Additional 525 ovicellate and non-ovicellate colonies, more poorly preserved than previous material; same details as the neotype; PMC Rosso-Collection I.H.B.115.b . France • 5 fragmentary colonies still attached to their substrate and some isolated detached autozooids including one with opposite regeneration. On fronds of L. rodriguezii , Mediterranean, Liguro-Provençal basin, NW Corsica, Ile-Rousse Bank ; coordinates not available; 85–100 m depth; 5 Aug. 1957; R/V Président Théodore Tissier survey, St. 423; J.-G. Harmelin leg.; PMC. Harmelin-Collection F.H.B.115.c .

Diagnosis.

Fenestrulina with smooth-rimmed, roundish ascopore, a simple distal process, a wide lumen centrally positioned within a markedly convex, smooth to finely granular frontal shield bordered by a row of small marginal pseudopores not extending proximally; ovicell smooth.

Description.

Colony encrusting algal fronds, multiserial, unilaminar, typically subcircular to slightly subelliptical (Figs 3 A , 5 A ), rarely lobate, up to ~ 7 mm in maximum dimension; initially consisting of concentric generations of alternating zooids, later becoming progressively irregular; interzooidal communications via pore-chambers: two proximolateral, two distolateral, one distal (~ 180 μm long) near base of vertical walls; pore-chamber windows fissure-like and barely visible (Fig. 4 F ) or subelliptical (Fig. 6 B – E ), usually masked by developing autozooids, even at colony periphery.

Autozooids ovoidal to rounded hexagonal, distinct, boundaries marked by narrow, deep grooves widening into subtriangular spaces at triple junctions (Figs 3 D – F , 4 , 5 B – D , 6 ). Lateral and proximal walls well exposed (50–70 μm wide), deeply sloping, in contact with neighbouring zooids only near base (Figs 4 , 6 ). Cryptocystidean frontal area bordered by a thin, raised rim of smooth calcification, typically straight distally just proximal to orifice (Fig. 4 A, C, D ), or with paired, short (~ 30 μm) lateral extensions (Figs 4 A – D , 5 F , 6 B – D ). Frontal shield convex, most elevated at ascopore level, smooth to finely, densely and evenly granular; perforated by fissure-like, semicircular to circular pseudopores, mainly adjacent to the edge of the slightly higher gymnocystal rim (Figs 3 C, E, F , 4 , 6 B – E , 23 A ), confined to the distal half to two-thirds of autozooid, numbering 12–20 ( 8–10 in periancestrular autozooids) (Fig. 5 ); area between orifice and ascopore with 5–10 additional pseudopores (2 or 3 in periancestrular autozooids). Pseudopores with 3–6 (usually 5) radial spiny processes centrally unjointed (Figs 4 B, C , 5 F , 23 A ). Two, rarely three, cryptocystidean areas with simple pores distal to orifice, interspersed among spines, soon concealed by distal autozooids (often covering oral spines as well), visible only at colony margin or in disjointed autozooids (Fig. 4 D ). Basal wall nearly uncalcified, except for a thin peripheral ring near vertical walls.

Primary orifice transversely D-shaped, hinge-line straight, with two minute denticles near proximal corners; distal rim slightly undulating to distinctly denticulated (Fig. 4 D ). Three, occasionally four, slender, weakly calcified tubular oral spines, up to ~ 130 μm long (base diameter 15–20 μm); proximalmost pair larger, positioned at mid-orifice length. Periancestrular autozooids usually with four oral spines, proximalmost pair occasionally bifurcated (Fig. 5 B , arrowed). In ovicellate zooids, spines reduced to two, always visible, adjacent to and often indenting lateral ovicell margin (Figs 3 D – F , 4 C, E , 5 D – F , 6 D ).

Ascopore centrally placed, ~ 80 μm proximal to orifice (Figs 3 E , 4 , 5 ), with a smooth rimmed subcircular, heart-shaped to transversely reniform lumen, featuring a simple to bifurcated distal process, occasionally subcircular (Fig. 5 B ); situated within a circular to transversely elliptical narrow field of smooth gymnocystal calcification, marked by a raised rim, laterally merging with the arched proximal rim of frontal shield in ovicellate zooids (Fig. 3 E, F ).

Ovicell subglobular, prominent, partially obscuring the distal part of the orifice, seemingly subcleithral and only partly closed by the operculum, produced by the distal autozooid (Fig. 3 D, E ). Endooecium calcified, smooth, rimmed by a row of 14–17 large, quadrangular pores separated by calcified ribs, creating a scalloped distal margin; narrowing proximally, with proximal rim folded upward into a thin protruding visor and extending into pointed lateral wings (Figs 4 C, E , 5 D – F ). Ectooecium mainly cuticular with a slightly raised rim of gymnocystal calcification along the proximal raised edge of the distal autozooid (Fig. 3 F ).

Ancestrula tatiform (Figs 5 A – C , 24 A ), oval, slightly smaller than periancestrular autozooids; gymnocyst more extensive proximally (~ 80 μm wide), tapering distally, rim sometimes undulating between 10 gymnocystal spines (five distal, more closely spaced than the equally spaced proximal ones). Cryptocystidean areas with simple pseudopores lateral to the distal triplet of spines, barely detectable. Ancestrula sometimes regenerating as miniature autozooids (Fig. 3 C ) or resembling a miniature autozooid without clear signs of regeneration (Fig. 5 D ). Budding pattern: one distal, two distolateral, two proximolateral, and one or two proximal zooids, totalling six or seven periancestrular autozooids, sometimes ovicellate (Fig. 3 C ).

Kenozooids not observed.

Remarks.

A notable character of F. malusii is the ascopore with a smooth rim and a wide cordiform to reniform lumen, unique among all species examined from the Mediterranean. A smooth-rimmed ascopore is clearly depicted in Savigny’s drawing of F. malusii (Fig. 1 ). When properly oriented, frontal views of ovicellate regions also reveal the same characters well illustrated in Savigny’s drawings, including the scarcity of pseudopores and their location, and the distal pores of the ovicell. These traits are particularly distinctive in the Mediterranean material, leading to the selection of this Fenestrulina population, and the best preserved colony within it, as the neotype for the species, in the absence of colonies from the original collection (see Introduction). A smooth-rimmed ascopore has been reported in some species from the Southern Hemisphere, such as F. cervicornis Hayward & Ryland, 1990 from the Ross Sea ( Antarctica), F. fritilla Hayward & Ryland, 1990 and F. jocunda Hayward & Ryland, 1990 , both from South Georgia and the former species also from Burdwood Bank (subantarctic region), and F. microstoma Moyano, 1983 from off the Chilean coast, north of Concepción, in the Pacific Ocean. In F. cervicornis , F. fritilla and F. microstoma , however, the lumen is subelliptical or slightly crescentic, while in F. jocunda , it is slit-like and mounted on an elevation ( Moyano 1983; Hayward and Ryland 1990; Hayward 1995). All these species strongly differ from F. malusii in several characters, such as the bifurcation or trifurcation of the proximalmost pair of oral spines in F. cervicornis , the absence of oral spines and the entirely pseudoporous frontal shield in F. fritilla , the large cribriform pseudopores of the frontal shield and the deeply pitted, wrinkled appearance of the ovicell endooecium in F. jocunda , and the almost entirely perforated frontal shield in F. microstoma ( Moyano 1983; Hayward and Ryland 1990; Hayward 1995). Broadly non-denticulate, but distinctly different, thin, slit-like C-shaped ascopores occur in F. thyreophora ( Busk, 1857) , a widespread, presumed highly variable southern hemisphere species.

Although roughly smooth surfaced, autozooids of F. malusii often show some granules, recalling those of Fenestrulina sp. , a still unnamed species from Safaga Bay in the Red Sea ( Ostrovsky et al. 2024; https://bryozoancollection.univie.ac.at/Sammlung/Bryozoa/Safaga_Bay/Cheilostomata/Microporellidae/Fenestrulina/Fenestrulina_sp.html). However, in that species, the granules are fewer and larger, the ascopore is C-shaped, its rim serrated, the frontal pseudopores differ in number, shape and location, and the ovicell lacks the folded proximal margin. A granular ornamentation of the frontal shield is also typical of the Mediterranean species F. granulosa sp. nov., which, however, also has a granular endooecium, more numerous trifoliate to quadrifoliate pseudopores arranged in three or four rows between the orifice and ascopore, extensive cryptocystidean lappets lateral to the orifice, a sporadic single distal oral spine, and a denticulate ascopore. The orifice is often distally obscured, with spines (especially the distal one) hidden by the swollen proximal portion of distal autozooids, which appear somewhat imbricated. Lateral walls sloping toward the organic substrate are largely exposed in this species, as seen also in F. epiphytica Hayward & Ryland (1995 : fig. 13 B, C). In our material, the substrate is sometimes partly exposed when autozooids remain unjointed, mostly at triple junctions (Fig. 4 D ). The spacing of autozooids, the connections through thin joints suggested by the commonly fissure-like windows in the lateral walls (Fig. 4 F ), the significant reduction or even absence of calcification in the basal walls (Figs 4 B, F , 5 F , 6 D, E ), and the apparent weak calcification of all walls (often leading to the collapse of autozooids in many colonies), especially at the margins where autozooids remain incompletely calcified (Fig. 5 A ), suggest functional adaptations for colonising flexible substrates. Colonies of this species have been found associated with L. rodriguezii fronds in high hydrodynamic environments of the Apollo Bank, off NW Sicily ( Di Geronimo et al. 1990), and the Ile-Rousse Bank, off NW Corsica. However, these adaptations also lead to the detachment of colonies, and even the disarticulation of individual autozooids, after colony death or in long-term preserved, desiccated colonies (Fig. 6 ). Loosely connected autozooids have also been observed in F. commensalis Viera & Stampar, 2014 as an adaptation to ensure flexibility and growth on its cerianthid host tube ( Vieira and Stampar 2014). Similarly, widely exposed lateral walls are also typical features of the possibly cryptogenic species F. delicia , mostly associated with the kelp Agarum cribrosum Bory, 1826 in the Gulf of Maine, though also reported from hard substrates (e. g., Winston et al. 2000; De Blauwe et al. 2014). Somewhat disjointed autozooids have been observed in F. granulosa sp. nov., also from flexible plant substrates, and in F. dictyota Hayward & Ryland, 1990 from Tristan da Cunha in the southern Atlantic Ocean.

The ancestrula can be a small autozooid but is usually tatiform and often regenerated as a miniature autozooid. In some cases, including the neotype (Fig. 3 ), central parts of colonies, where autozooids radiate, show regeneration, with some autozooids exhibiting varying degrees of damage and repair. In these cases, the ancestrula is difficult to identify as two centrally located modules with opposite polarity (with or without signs of regeneration) are present. In two cases documented via SEM, an ovicellate autozooid is adjacent to one of these modules (Fig. 3 C ). Interestingly, F. malusii exhibits three out of four types of ancestrulae typical of the genus, i. e., simply tatiform, tatiform regenerated as a miniaturised autozooid, or a small autozooid-like ancestrula.

Ovicells are notably large relative to autozooids, as indicated by the low ZOvL / OvL ratio (2.15). Variability is evident in the shape (length / width) and size of autozooids, with some abnormalities observed, such as disproportionately large ovicells and deformed maternal and distal autozooids producing the ovicell (e. g., Fig. 5 E, F ). In one instance, an extremely large autozooid with a dimorphic large orifice was observed at the colony margin, likely resulting from the fusion of two contiguous autozooids, as indicated by the presence of two ascopores and a bifid proximal margin with caudal extensions budded from the preceding autozooid. This may be due to the failure of a zooidal row bifurcation. Similar deformities have also been noted in F. communis sp. nov. The occurrence of numerous ovicells (e. g., Fig. 3 A, D ) in all examined colonies, despite their small size (Fig. 5 A ), and their early formation, even in periancestrular autozooids or those immediately subsequent (Figs 3 B, C , 5 A, D ), represents a reproductive strategy of this species. These observations in colonies collected during summer align with Bishop’s (1989) theory on the early production of ovicells for larval incubation and release in “ spot colonies ”, a strategy typical of r-selected species colonising ephemeral substrates, such as seasonally developing algae and / or small, unstable substrates (e. g., Rosso et al. 2014). In this case, the distal (older) parts of Laminaria blades, which grow seasonally from the base, are prone to senescence and / or breakage / removal by mechanical forces and feeding activity by organisms.

Habitat distribution.

All colonies of F. malusii examined have been found on the large, flat, and smooth blades of the fleshy alga L. rodriguezii , collected from a rocky elevation swept by strong bottom currents, at a depth of ~ 60 m, where a particular facies of the Coralligenous biocoenosis develops owing to the local transparency of the water, allowing deep light penetration ( Di Geronimo et al. 1990). A few additional colonies originated from Laminaria fronds collected off Ile-Rousse, Corsica, at 85–100 m depth. The species was first drawn on a frond of S. vulgare by Savigny (1817), indicating a preference for flexible substrates. In contrast, the possible association of F. malusii with Posidonia meadows currently reported in ecological literature relating to the Mediterranean, remains to be ascertained.

Geographical distribution.

Although widely reported from the Mediterranean (and in the Atlantic), after the examination of a great number of colonies and images, we currently confirm the occurrence of F. malusii from only two localities: the Apollo Bank near Ustica Island in the SW Tyrrhenian Sea, and a Laminaria bank off Ile-Rousse, NW Corsica, in the Liguro-Provençal basin. However, the geographical distribution of the species may be wider than currently recognised, as indicated by its occurrence on Laminaria , which in the Mediterranean can extend to relatively deep waters (~ 100 m), habitats that are less frequently explored. Current presence off the Egyptian coast, site of original description, remains unconfirmed.

Figures

Figure 1. Geographical distribution of Mediterranean Fenestrulina species (and specimens) examined in this study. Asterisks denote newly described species and the only confirmed record of Fenestrulina malusii (Audouin & Savigny, 1826), illustrated here with Savigny’s original drawing (reproduced from d’Hondt 2006) shown on the left. Type material is shown for each species, except for F. malusii, for which the neotype (upper image) and a colony fragment from Ile-Rousse Bank, NW Corsica (lower image) are figured. Large symbols indicate type localities; small symbols mark additional occurrences. Symbol colours correspond to species as follows: red = F. malusii; bright green = F. cavernicola sp. nov.; vivid pink = F. communis sp. nov.; pale blue = F. foveolata sp. nov.; blue = F. granulosa sp. nov.; olive green = F. kalliste sp. nov.; dark green = F. ovata sp. nov.; purple = F. variorugosa sp. nov.; lilac = Fenestrulina sp. Note: in areas with multiple records, only one symbol is used to represent the locality.

Figure 3. Fenestrulina malusii (Audouin & Savigny, 1826) neotype PMC. B 37. Neotype. 23. 2. 2024. a, Apollo Bank, Ustica Island, Tyrrhenian Sea. A. General view of the colony, largely composed of ovicellate autozooids; B. Central zone with non-ovicellate autozooids, encircled by rings of ovicellate ones; C. Enlargement of the framed area in B, showing the ancestrula regenerated as a miniature autozooid, and surrounding periancestrular autozooids, one of which is ovicellate (asterisk); D. Colony periphery, almost entirely composed of ovicellate autozooids; E. A single non-ovicellate autozooid surrounded by ovicellate ones. Note the reniform, smooth ascopore with a tiny distal process; F. Developing ovicell. Scale bars: 1 mm (A, B); 200 μm (C, E, F); 500 μm (D).

Figure 4. Fenestrulina malusii (Audouin & Savigny, 1826) Apollo Bank, Ustica Island, Tyrrhenian Sea. A, D. PMC. Rosso Coll. I. H. B. 115. a 2; B, C, F. PMC. Rosso Coll. I. H. B. 115. a 3; E. PMC. Rosso Coll. I. H. B. 115. a 5. A. Non-ovicellate autozooids from the colony centre, showing few pseudopores; B. Non-ovicellate autozooid from the colony periphery, with more numerous pseudopores; C. Inclined ovicellate autozooids showing the proximal constriction of the ovicell and its upward-folding rim; D. Autozooid showing the orifice with a finely and irregularly denticulate distal margin and a straight proximal margin bearing two tiny denticles. Note the substrate exposed between the loosely spaced autozooids; E. Colony margin with developing autozooids; F. Fissure-like pore chambers along the distolateral wall of an autozooid. In panels B, C, and E note the long, weakly calcified oral spines. Scale bars: 200 μm (A – C, E); 100 μm (D, F).

Figure 5. Fenestrulina malusii (Audouin & Savigny, 1826) Apollo Bank, Ustica Island, Tyrrhenian Sea. A, B. PMC. Rosso Coll. I. H. B. 115 a 1; C. PMC. Rosso Collection I. H. B. 115 a 2; D. PMC. Rosso Coll. I. H. B. 115. a 6; E. neotype PMC. B 37. Neotype. 23. 2. 2024; F. PMC. Rosso Coll. I. H. B. 115. a 4. A. Colony showing a ring of ovicellate autozooids surrounding the first generations of non-ovicellate autozooids near the ancestrula; B. Detail of the ancestrula and six periancestrular autozooids in panel A. Arrows indicate bifurcated spines; C. Tatiform ancestrula surrounded by seven irregularly budded and partly regenerated autozooids; D. Ancestrula regenerated as a miniature autozooid. Note the early development of ovicells; E. Zone of ovicellate autozooids with only three non-ovicellate ones, showing shape variability, and an abnormal autozooid producing a large ovicell; F. Large teratological autozooid with a wide orifice and two drop-shaped ascopores, resulting from the fusion of two contiguous autozooids, as indicated by the morphology of the proximal margin. Scale bars: 1 mm (A); 500 μm (B – E); 200 μm (F).

Figure 6. Fenestrulina malusii (Audouin & Savigny, 1826) PMC Harmelin Coll. I. H. B. 115. c, Ile-Rousse Bank, NW Corsica, Liguro-Provençal basin. A. Fragment of a Laminaria frond with some autozooids (two enlarged in panel E) still attached, indicating the remnants of a once larger colony. Note the co-occurrence of F. variorugosa sp. nov. and other bryozoans: Cb = Chorizopora brongniartii (Audouin & Savigny, 1826); Fm = F. malusii; Fv = F. variorugosa sp. nov.; Hf = Hippothoa flagellum Manzoni, 1870; B, C. Close-ups of two autozooids from the colony fragment in panel D, showing elongate pore chambers along distal and distolateral walls; D. Group of autozooid, including one ovicellate; E. Two autozooid from the colony in panel A, one regenerated with reversed polarity; F. Isolated detached autozooid with a regenerated ascopore zone. Scale bars: 1 mm (A); 100 μm (B, C); 200 μm (D – F).

Figure 22. Geographical distribution of all known records of Fenestrulina in the Mediterranean, plotted against current summer Sea-Surface Temperatures (data from IFREMER-LOPS Data Visualization Portal https://syntool.ifremer.fr/, accessed Sept. 2024). An asterisk marks the probable origin of the original material of F. malusii. Large dots: collection sites of specimens with confirmed species attribution; small dots: records of putative F. malusii requiring taxonomic revision, but with known provenance; open ellipses: sites, covered by dedicated monographs, from which Fenestrulina species are absent.

Figure 23. Comparison of pseudopores in the studied species of Fenestrulina. A. F. malusii; B. F. cavernicola sp. nov.; C. F. communis sp. nov.; D. F. foveolata sp. nov.; E. F. granulosa sp. nov.; F. F. kalliste sp. nov.; G. F. ovata sp. nov.; H. F. variorugosa sp. nov.; I. Fenestrulina sp. Scale bars: 100 μm.

Figure 24. Comparison of ancestrulae in the studied species of Fenestrulina. A. F. malusii, tatiform; B. F. cavernicola sp. nov., regenerated as a kenozooid; C. F. communis sp. nov., tatiform; D. F. communis sp. nov., regenerated as a miniature autozooid; E. F. foveolata sp. nov., tatiform; F, G. F. variorugosa sp. nov., tatiform. Scale bars: 200 μm.