Pentapora, FISCHER, 1807

Lombardi, Chiara, Taylor, Paul D. & Cocito, Silvia, 2010, Systematics of the Miocene-Recent bryozoan genus Pentapora (Cheilostomata), Zoological Journal of the Linnean Society 160 (1), pp. 17-39 : 18-26

GENUS PENTAPORA FISCHER, 1807

Type species: Millepora foliacea Ellis & Solander, 1786 . Subsequent designation by Hastings & Ryland (1968).

Revised diagnosis: Colony multiserial, encrusting unilamellar or multilamellar, or more often attached by an encrusting base, but developing erect bifoliate branches to form a domed meandriform structure comprising anastomosed and folded laminae (eschariform), or a bushy colony with strap-like bifurcating branches (adeoniform). Colour white or pale orange in encrusting species, deep orange in erect species, fading to pale after death; embryos and larvae pale in colour.

Autozooids oval to rectangular or rounded hexagonal, arranged quincuncially. Frontal shield lepralioid, flat or slightly convex, initially finely granular but becoming rugose, wrinkled, or knobbly as a result of secondary calcification; evenly porous, with marginal areolar pores and central pseudopores of similar size, deepening and often becoming obscured by secondary calcification. Interzooidal boundary walls salient in young zooids, often covered by secondary calcification in older zooids. Orifice longer than wide, rectangular to semi-elliptical with the proximal margin straight, slightly concave, or convex, and bearing a small mucro; oral spines absent or present, typically lost or overgrown during late ontogeny; lappets (lateral pro- longations of the orificial rim) variably developed, when pronounced producing trifoliate secondary orifice. Condyles present, typically small and downwardly curved, dividing the primary orifice into a large anter and a smaller poster. Operculum pale brown, translucent, with marginal sclerites. Short median septum developed on basal walls at proximal ends of zooids in all but one species. Multiporous septula present in lateral and transverse vertical walls. Ovicell hyperstomial, as wide as long, usually globose or flat; closed by the operculum; porous, either a single central pore or multiple pores scattered over surface of ooecium, or arranged in an arc above orifice, enveloped by secondary calcification in most species; lappets generally better developed in fertile zooids, occasionally forming a complete bridge above the orifice.

Avicularia adventitious, suboral, not present on all zooids; placed on the umbo, directed proximally, varying from acute to almost normal to the frontal plane; rostrum rounded, crossbar calcified. Normalsized avicularia occasionally replaced by giant avicularia with spatulate or subtriangular rostrum, crossbar uncalcified or calcified with or without a columella, occasionally covered by closure plate.

Remarks: Pentapora was introduced by Fisher (1807) to replace Eschara sensu Lamarck, 1801 non Linnaeus, 1758. Fisher included four species in his new genus: Millepora foliacea Ellis & Solander, 1786 , Millepora taenialis Ellis & Solander, 1786 , Millepora cervicornis Ellis & Solander, 1786 , and Pentapora tubulata sp. nov. The genus was then neglected for more than 150 years. For example, Pentapora is not mentioned in three standard compilations of bryozoan names ( Jelly, 1889; Bassler, 1935, 1953). It was left to Hastings & Ryland (1968) to revive Pentapora , and to select M. foliacea as the type species. According to these authors, M. taenialis is a variety of the type species, P. tubulata is unrecognizable, and M. cervicornis belongs in either Porella or Smittina .

PENTAPORA FOLIACEA ( ELLIS & SOLANDER, 1786)

( FIGS 1A , 2 , 3 )

Millepora foliacea: Ellis & Solander, 1786: 133 .

Pentapora foliacea: Fischer, 1807: 307 ; Hastings & Ryland, 1968: 506 (part), Figure 1A–D, F–M ; Hayward & Ryland, 1979: 94 (part), figs 32, 33A;? Bishop, 1987: 13, figs 22–25.

Eschara foliacea Lamarck, 1801: 375 ; Milne-Edwards, 1836: 34–38, pl. 3, fig. 1; Busk, 1854: 89.

?Eschara bidentata Milne-Edwards, 1836: 38, pl. 3, figs 2, 2a.

Eschara foliacea: Johnston, 1847: 350 , pl. 67, figs 1–5.

Lepralia foliacea: Hincks, 1879: 159 ; Hincks, 1880: 300, pl. 31, fig. 3, pl. 47, figs 1–4; Waters, 1879: 124, pl. 15, fig. 8; Jelly, 1889: 127; Waters, 1891: 273, pl. 29, figs 1–3; Calvet, 1900: pl. 13, fig. 20; Waters, 1925: 657, pl. 36, fig. 5.

Hippodiplosia foliacea :? Canu & Bassler, 1925: 31, pl. 7, figs 8–9;? Canu & Bassler, 1928: 34, pl. 3, fig. 11; Canu & Bassler, 1930: 50, pl. 6, figs 1–2; Balavoine, 1956: 35, pl. 1, figs 1–6, pls 2, 3.

? Hippodiplosia otto-mulleriana: Lagaaij, 1952: 80 , pl. 7, figs 5, 6.

Pentapora fascialis: Hayward & Ryland, 1999: 200 (part), figs 79, 80A, 81A–B.

Material examined: NHM 1897.5.1.813, Portugal, Bracebridge Wilson Collection. NHM 1897.5.1.812, 1897.5.1.815, Hastings, Kent. 99.5.1.808, Isle of Man, Hincks Collection. NHM 99.7.1.1415, Lisbon, Busk Collection. NHM 99.7.1.4903, Weymouth , Busk Collection. NHM 99.7.1.1418, Dartmouth , Busk ex Forbes Collection. NHM 11.10.1.1566, Guernsey, 1865. NHM 11.10.1.1561, Cornwall. NHM 11.10.1.1566, Guernsey, Norman Collection , 1865. NHM 11.10.1.1560, The Minch , Hebrides, Norman Collection , 1866. NHM 19.6.25.93, Guernsey, Norman Collection. NHM 25.4.21.2, cable 10 miles north-west of Scilly Island , 40 fathoms, Wilson Collection. NHM 1964.4.8.1, 2 miles off Gull Rock , Portscantho , Cornwall, 20 fathoms, Nicholas & Lane Collection. NHM 1965.8.20.20, La Chapelle Bank. NHM 1967.8.5.1, Martin’s Haven , Pembrokeshire, illustrated by Hastings & Ryland (1968, Fig. 1A–D, F–M ). NHM 1967.8.5.1, Martin’s Haven , Pembrokeshire, 18 m, 1958. NHM 1975.7.18.2, Herm , Channel Islands , Lagaaij Collection , 1973. NHM 1985.1.10.54, Boreray , St Kilda , Hayward Collection , July 1979. NHM 1997.9.24.2, off Eddystone Light , 60 m, Tilbrook Collection , May 1994. NHM 2009.1.28.1, growing on French Atlantic Cable , 60 miles west of Brest , 60–70 fathoms, Manger Collection. NHM 2009.1.28.2, ~ 8 miles south of Littlehampton , Sussex , 20 m, Mitchell Collection , November 2001. NHM 2007.9.14.2, Persier Reef , Devon, 50°17.107 ′ N, 3°58.056 ′ W, 24 m, Lombardi & Hiscock Collection, August 2005. NHM 2007.9.14.4, Skomer Nature Reserve , Watwick, Dyfed, Wales, 51°41.736 ′ N, 5°8.989 ′ W, Lombardi Collection, August 2006. NHM 2007.9.14.5, Bardsey Island , North Wales, 54°45.095 ′ N, 4°47.260 ′ W, Tompsett Collection. NHM 2007.9.14.13, Flat Ledges, Scilly Islands , 49°58.035 ′ N, 6°15.215 ′ W, Porter Collection, May 2007. NHM 2009.1.28.1, British waters, no details .

Revised diagnosis: Pentapora with foliaceous, box-like colonies; autozooids large, averaging 0.81-mm long by 0.36-mm wide; avicularia monomorphic, small; ovicell with pores in a band close to orifice.

Description: Colonies developing three-dimensional, box-like growths comprising folded and anastomosing bilamellar plates from an extensive encrusting base. Early astogeny unknown.

Autozooids longer than wide, 0.67–0.93 mm long (mean 0.81 ± 0.09 mm; N = 20) by 0.28–0.44 mm wide (mean 0.36 ± 0.04 mm; N = 20), roughly rectangular in shape, initially elongate, but becoming more equidimensional during ontogeny ( Hayward & Ryland, 1999); arranged quincuncially; zooidal boundary walls salient. Frontal shield lepralioid, granular, with areolar pores and pseudopores, both becoming less distinct through wall thickening during ontogeny, which also obscures zooidal boundaries. Primary orifice 0.11–0.20 mm long (mean 0.18 ± 0.02 mm; N = 15) by 0.16–0.19 mm wide (mean 0.18 ± 0.01 mm; N = 15), a pair of downturned condyles between anter and poster; secondary orifice slightly oval to trifoliate because of the development of lappets. Operculum brown, lustrous. No oral spines. Basal walls with short median septum extending distally from transverse wall ( Fig. 2B , marginal zooids). Multiporous septula in lateral and transverse vertical walls near their bases; circular to ovoidal shallow muscle impressions may be visible close to septula. Ovicell elliptical, wider than long, 0.21–0.25 mm long (mean 0.23 ± 0.01 mm; N = 20) by 0.27–0.35 mm wide (mean 0.31 ± 0.02 mm; N = 20), a few scattered pores arranged in a band proximally above orifice, becoming overgrown by secondary calcification.

Avicularia monomorphic, adventitious, suboral, usually placed on an umbo, inconspicuous, small, longer than wide, 0.09–0.11 mm long (mean 0.100 ± 0.005 mm; N = 10) by 0.08–0.10 mm wide (0.090 ± 0.007 mm; N = 10); rostrum semielliptical; orifice 0.050 ± 0.005 mm long by 0.030 ± 0.004 mm wide; crossbar averaging 0.060 ± 0.008 mm long. Giant avicularia not observed, presumed lacking.

Remarks: The neotype specimen of M. foliacea Ellis & Solander, 1786 , reputedly present in the NHM collections, was actually destroyed at the Royal College of Surgeons during World War II (M. Spencer Jones, pers. comm.). Neither an illustration of M. foliacea nor a type locality were given by Ellis & Solander, but they reported that the species was distributed commonly around the British coast, citing Ellis (1755) and Linnaeus (1758). Ellis (1755, pl. 30, figs a, A–C) illustrated the species from the Isle of Wight, prompting Hastings & Ryland (1968) to choose this illustration as the lectotype of P. foliacea .

The large and striking colonies of P. foliacea have long attracted the attention of naturalists, and are a familiar sight to divers around the west and south coasts of Britain today ( Fig. 1A ). As noted above, the relationships between this Atlantic species and the Mediterranean P. fascialis are uncertain: some authors have regarded them as distinct species, whereas others have considered them to be synonyms. The final answer may depend on molecular analysis. For the purpose of the present paper, P. foliacea and P. fascialis are described separately. Apart from their provenance, the typically bifurcating branches of P. fascialis and the presence of giant avicularia are the best means of differentiating between the two species. In addition, the secondary thickening of the frontal shield is generally greater in P. fascialis than in P. foliacea ( Figs 2A , 3B ). As pointed out by Hayward & Ryland (1979), Eschara bidentata Milne-Edwards, 1836, is an ontogenetic variety of P. foliacea in which the lappets are particularly well developed.

Pliocene fossils from the Scaldisian (late Zanclean to Piacenzian) of Wilmarsdonk, Belgium, lacking giant avicularia, and assigned by Lagaaij (1952) to Hippodiplosia ottomulleriana (Moll) (see below), were reidentified as P. foliacea by Bishop (1987). This identification is provisionally accepted here, although it should be noted that the small fragments available for study raise the possibility of giant avicularia being present but remaining undetected in this population of Pentapora .

Distribution: Recent: north-eastern Atlantic from St Kilda in the north to the coast of Morocco in the south, including the English Channel as far east as Hastings; Mediterranean occurrences, which are seldom adequately described in the literature, require reassessment in view of the close similarities between P. foliacea and P. fascialis . Fossil: questionably, Pliocene (late Zanclean–Piacenzian), Belgium ( Bishop, 1987).

PENTAPORA FASCIALIS ( PALLAS, 1766)

( FIGS 1B , 4–6 )

Eschara fascialis: Pallas, 1766: 42 .

Eschara foliacea Milne-Edwards, 1836: 34 , pl. 3, fig. 1; Manzoni, 1870: 18, pl. 4, fig. 4; Manzoni, 1876, pl. 5, fig. 6.

Lepralia foliacea Hincks, 1879: 159 ; Hincks, 1880: 300, pl. 47, figs 1–4; Waters, 1879: 124, pl. 15, fig. 8; Waters, 1891: 273, pl. 19, figs 1–3; Calvet, 1900: pl. 13, fig. 20; Waters, 1925: 657, pl. 36, fig. 5.

Hippoporina foliacea Neviani, 1939: 51 .

‘Hippodiplosia’ fascialis Gautier, 1952: 164 .

Pentapora foliacea Hastings & Ryland, 1968: 506 (part), fig. 1E only; Hayward & Ryland, 1979: fig. 33B.

Pentapora fascialis Zabala, 1986: 401 , fig. 132; Zabala & Maluquer, 1988: 115, figs 238–239, pl. 8, fig. E; Hayward & Ryland, 1999: 200 (part), fig. 80B only; Hayward & McKinney, 2002: 53, fig. 25A–E.

Pentapora fascialis fascialis Chimenz, Rosso & Balduzzi, 2005: 5 .

Material: Recent: NHM 34.2.20.15, Port Western, South Australia , Busk Collection. NHM 1879.4.25.2, Naples , Italy, Waters Collection. NHM 79.4.25.53, 97.5.1.864, Naples , Waters Collection. NHM 96.12.2.2, Marseille , Vayssière Collection. NHM 99.7.1.1417, 99.7.1.4907, coast of Spain, Busk Collection. NHM 99.7.1.29, Mediterranean , Busk Collection. NHM 1963.9.4.8, Oran, Algeria, 54 fathoms, Waters- O’Donoghue Collection. NHM 1965.9.2.21, Station 228, Mediterranean , Gautier Collection. NHM 2001.1.25.4, near Marseille , Warren Collection , 1975. NHM 1975.1.12.384, Emborios Cave , Chios , Greece, 50 feet, Hayward Collection , August 1967 . NHM 2007.9.14.14, Tino Island, Italy, 44°17.68 ′ N, 9°50.88 ′ E, Lombardi & Cocito Collection , July 2007 .

Fossil: NHM BZ 5664-8, Pliocene, Emilian, Gillima, Calabria, Italy, Toscano Collection. NHM BZ 5672-4, Middle Pliocene, Castell’Arquato, Piacenza, Emilia, Italy, Pizzaferri Collection. NHM BZ 5669-71, Lower Pleistocene, Arda stream, Castell’Arquato, Piacenza, Emilia, Italy, Pizzaferri Collection.

As far as can be ascertained (e.g. Kuklinski & Taylor, 2008), the type material of bryozoans described by Pallas (1766), including Eschara fascialis , has been lost.

Revised diagnosis: Pentapora with colonies of narrow, bifurcating branches; autozooids large, averaging 0.88 mm long by 0.42 mm wide, frontal shield thickly calcified; avicularia dimorphic, the giant avicularia spatulate; ovicell with a few scattered pores.

Description: Colonies developing erect, narrow, straplike, bifurcating branches from an encrusting base. Early astogeny unknown.

Autozooids longer than wide, 0.68–1.28 mm long (mean 0.88 ± 0.13 mm; N = 20) by 0.32–0.54 mm wide (mean 0.42 ± 0.05 mm; N = 20) in recent samples, 0.73–0.79 mm long (mean 0.75 ± 0.03 mm; N = 20) by 0.44–0.48 mm wide (mean 0.46 ± 0.02 mm; N = 20) in Pliocene fossils, roughly rectangular in shape, arranged quincuncially with distinct boundaries becoming obscured during later ontogeny. Frontal shield lepralioid, granular, with areolar pores and pseudopores, developing knobs as thickening increases during ontogeny. Primary orifice 0.17– 0.25 mm long (mean 0.21 ± 0.02 mm; N = 20) by 0.14–0.21 mm wide (mean 0.18 ± 0.01 mm; N = 20) in recent material, 0.13–0.19 mm long (mean 0.17 ± 0.02 mm; N = 20) by 0.11–0.17 mm wide (mean 0.15 ± 0.02 mm; N = 20) in Pliocene fossils, a pair of downturned condyles between anter and poster; secondary orifice slightly oval to trifoliate, following the development of lappets. Operculum brown, lustrous. Oral spines lacking in recent material, but very occasionally observed lateral to the orifice in Pliocene fossils. Basal walls with short median septum extending distally from transverse wall. Multiporous septula present in lateral and transverse vertical walls. Ovicells globular or elliptical, wider than long, 0.19–0.25 mm long (mean 0.22 ± 0.01 mm; N = 20) by 0.24–0.35 mm wide (mean 0.32 ± 0.03 mm; N = 20) wide, pores few, scattered, becoming occluded by secondary calcification.

Avicularia dimorphic, adventitious, suboral, proximally directed. Normal avicularia small, inclined at a high angle to frontal surface, longer than wide, 0.08– 0.12 mm long (mean 0.09 ± 0.01 mm; N = 10) by 0.07– 0.09 mm wide (mean 0.08 ± 0.003 mm; N = 10) in recent material, 0.08–0.11 mm long (mean 0.09 ± 0.01 mm; N = 10) by 0.07–0.09 mm wide (mean 0.08 ± 0.01 mm; N = 10) in Pliocene fossils; rostrum short, semielliptical; orifice 0.050 ± 0.005 mm long (N = 10) by 0.030 ± 0.007 mm wide (N = 10); crossbar averaging 0.050 ± 0.004 mm long (N = 10). Giant avicularia occasionally replacing normal avicularia; longer than wide, 0.29–0.42 mm long (mean 0.34 ± 0.07 mm; N = 5) by 0.17–0.20 mm wide (mean 0.11 ± 0.01 mm; N = 5) in recent material, 0.26–0.41 mm long (mean 0.32 ± 0.05 mm; N = 5) by 0.13–0.23 mm wide (mean 0.18 ± 0.05 mm; N = 5) in Pliocene fossils; rostrum spatulate, palate deep; orifice 0.13 ± 0.04 mm long by 0.070 ± 0.001 mm wide (N = 5); crossbar averaging 0.110 ± 0.001 mm long (N = 5).

Remarks: Autozooid morphology in the Mediterranean species P. fascialis is identical to the North Atlantic species P. foliacea , although frontal shield thickness can be greater in the former species. This has led many authors to regard them as synonyms. Although P. foliacea always constructs foliaceous colonies composed of broad fronds (eschariform) ( Fig. 1A ), colonies of P. fascialis typically comprise narrow, bifurcating, strap-like branches (adeoniform) ( Fig. 1B ). However, some populations of P. fascialis may also develop foliaceous colonies. Foliaceous and strap-like branches are even occasionally present within single colonies ( Cocito & Ferdeghini, 2000), suggesting ecophenotypic control of colony form. Indeed, Cocito & Ferdeghini (2000) studied a population from the Gulf of Spezia, in the Ligurian Sea, in which colonies growing in unidirectional flow regimes were foliaceous, whereas those in more turbulent habitats had broad laminae in the upstream parts of colonies, but narrow strap-like branches in downstream parts. On the other hand, giant avicularia have only ever been found in Mediterranean P. fascialis (e.g. Fig. 5B ); they are unreported from P. foliacea in the North Atlantic. Although the development of giant avicularia in Pentapora may also be under ecophenotypic control, such avicularia can be useful in discriminating between closely related cheilostome species ( Lombardi et al., 2008). Therefore, we here treat P. fascialis and P. foliacea as separate species pending the availability of molecular data. The cladistic analysis below offers some support for the distinction of P. fascialis and P. foliacea , in that they are separated by the Pliocene Pentapora lacryma sp. nov. in our phylogenetic analysis.

Hayward & McKinney (2002: 54) described the lophophores of Adriatic P. fascialis thus: ‘Tentacles light orange, 17–19; lophophore bell-shaped, radially symmetrical away from colony edge, obliquely truncate along colony margins and locally (at chimneys?) on colony surface.’

Distribution: Recent: Mediterranean Sea, from the Strait of Gibraltar in the west to the Aegean in the east. Specimens ( NHM 34.2.20.15) reputedly from South Australia exactly match the Mediterranean P. fascialis ( Fig. 5E–F ). If the provenance is correct, this represents a distant geographical outlier, likely to have resulted from an anthropogenic introduction of the species. Perhaps significantly, the South Australian material contains tiny inferred predator borings of a type not observed in Mediterranean populations, but like those known from Australian bryozoans belonging to other species (P. Bock, unpubl. data). Fossil: Middle Pliocene–Lower Pleistocene, Emilia and Calabria, Italy ( Fig. 6A–F ).

Figures

Figure 1. Large colonies of the cheilostome bryozoan Pentapora. A, eschariform colony of Pentapora foliacea (Ellis & Solander, 1786), British waters, NHM 2009.1.28.3. B, adeoniform colony of Pentapora fascialis (Pallas, 1766), NHM 2001.1.25.4, near Marseille. Scale bars: A = 4 cm; B = 2 cm.

Figure 2. Pentapora foliacea (Ellis & Solander, 1786), Skomer Nature Reserve, Watwick, Dyfed, Wales, NHM 2007.9.14.5; scanning electron micrographs of coated specimens imaged using secondary electrons. A, old autozooids. B, growing edge and a kenozooid (left of centre). C, primary orifice. D, ovicellate zooids. E, autozooids, many with small suboral avicularia. F, oblique profile of suboral avicularium. Scale bars: A, B = 0.4 mm; C = 150 Mm; D, E = 0.4 mm; F = 40 Mm.

Figure 3. Pentapora foliacea (Ellis & Solander, 1786); scanning electron micrographs of uncoated specimens imaged using back-scattered electrons. A–C, NHM 2009.1.28.2, Littlehampton, Sussex, England. A, young autozooids close to growing edge. B, older autozooids. C, primary orifice of a young autozooid. D, primary orifice, Boreray, St Kilda, Scotland, NHM 1985.1.10.54. E–F, Persier Reef, Plymouth, Devon, England, NHM 2007.9.14.2. E, young ovicell. F, older ovicell embedded in secondary calcification. Scale bars: A = 290 Mm; B = 180 Mm; C, D = 60 Mm; E, F = 100 Mm.

Figure 4. Pentapora fascialis (Pallas, 1766), Tino Island, Italy, NHM 2007.9.14.14; scanning electron micrographs of coated specimens imaged using secondary electrons. A, autozooids. B, growing edge. C, primary orifice. D, oblique profile of normal suboral avicularium. Scale bars: A = 0.5 mm; B = 0.4 mm; C = 100 Mm; D = 0.5 mm.

Figure 5. Pentapora fascialis (Pallas, 1766), scanning electron micrographs of uncoated recent specimens imaged using back-scattered electrons. A, B, Tino Island, Italy, NHM 2007.9.14.14. A, group of autozooids, some with ovicells. B, autozooidal orifice and giant suboral avicularium. C, D, Oran, Algeria, NHM 1963.9.4.8. C, edge of branch showing autozooids (most with normal suboral avicularia) and marginal kenozooids. D, orifice and normal suboral avicularium. E, F, reputedly from Port Western, South Australia, NHM 34.2.20.15. E, inferred predator boreholes (arrowed) in frontal shields. F, giant suboral avicularia. Scale bars: A = 280 Mm; B = 100 Mm; C = 470 Mm; D = 60 Mm; E = 300 Mm; F = 100 Mm.

Figure 6. Pentapora fascialis (Pallas, 1766), scanning electron micrographs of uncoated fossil specimens imaged using backscattered electrons. A–C, Lower Pleistocene, Arda stream, Castell’Arquato, Piacenza, Emilia, Italy, NHM BZ 5669. A, colony fragment showing zooids with normal and giant avicularia, and ovicells overgrown by secondary calcification. B, giant avicularium in autozooid having primary orifice almost obscured by lappets forming a bridge. C, ovicell. D–F, Pliocene, Emilian, Gillina, Calabria, Italy. D, E, NHM BZ 5664. D, autozooids, showing normal avicularia and a giant avicularium, and a broken ovicell. E, ovicell. F, NHM BZ 5667. bases of oral spines (arrows). Scale bars: A = 300 Mm; B = 150 Mm; C, E = 120 Mm; D = 200 Mm; F = 110 Mm.