Cribrilinids (Bryozoa, Cheilostomata) associated with deep-water coral habitats at the Great Bahama Bank slope (NW Atlantic), with description of new taxa Author Rosso, A. Author Beuck, L. Author Vertino, A. Author Sanfilippo, R. Author Freiwald, A. text Zootaxa 2018 2018-11-23 4524 4 401 439 journal article 27918 10.11646/zootaxa.4524.4.1 4a1c96f6-d406-4b11-8a10-3c7c415e4e47 1175-5326 2610612 22A47EBE-338A-4AAF-A63F-45EDE9727F18 Glabrilaria hirsuta Rosso n. sp. ( Figs 10–38 ; Tables 1 , 2 ) Material examined. Holotype : Great Bahama Bank slope, R/ V Maria S. Merian Cruise MSM20 /4, Station GeoB16374-1 one live, fertile colony encrusting a coral branch and including the ancestrula)—SMF-45.505 . Paratypes : Great Bahama Bank Slope, R / V Maria S. Merian Cruise MSM20 /4. Station GeoB16367-2 (two live and 20 dead colonies, all on corals, except for three on erect bryozoans, one on a serpulid, and one on a barnacle plate) – SMF-45.506; Station GeoB16368-1 (one dead colony on a coral)—SMF-45.507; Station GeoB16375-1 (31 dead colonies on corals)—SMF-45.508; Station GeoB16376-1 (3 dead colonies on corals)—SMF-45.509; Station GeoB16377-1 (one living and 12 dead colonies on corals, except for one on a fragment of sponge skeleton)—SMF- 45.510; Station GeoB16378-1 (one dead colony on a coral branch)—SMF-45.511; Station GeoB16382-1 (nine living and 30 dead colonies on corals)—SMF-45.512; Station GeoB16388-3 (one living plus two dead colonies on corals)—SMF-45.513 . FIGURES 10 , 11. Glabrilaria hirsuta Rosso n. sp. , Great Bahama Bank slope, Station GeoB16374-1, holotype SMF-45.505a. 10. Composed image of a colony forming an almost complete ring around a coral branch about 5 mm in diameter. Two relatively long pauciserial lobes diverge from the ancestrula (arrowed in the second and third part of the composite image). 11. Strongly inclined view of some autozooids to show their typical spiny appearance. Scale bars: 10 = 1 mm; 11 = 200 µm. FIGURES 12–18. Glabrilaria hirsuta Rosso n. sp. , Great Bahama Bank slope, Station GeoB16374-1, holotype SMF-45.505a. 12. Marginal autozooid with bases of six oral spines, surrounded by kenozooids. 13. Ovicellate zooid with bases of four oral spines and an avicularium on one side. Note the transversal spiny crest surrounding the crescent-shaped flat and steeply inclined proximal surface of ectooecium. 14. Slightly inclined view of a peripheral ovicellate zooid with two avicularia lateral to the orifice and very prominent spiny processes of the ovicell crest. 15, 16. Inclined distal views of two ovicells showing the spiny crests of the ooecia and the costate distal shields of the ooecium-bearing kenozooids. 17. Periancestrular area showing the asymmetrical budding pattern of autozooids and kenozooids only from one side of the ancestrula; note that some autozooids posses seven oral spines. 18. Ancestrula with the bases of six articulated oral spines, three pairs of more spaced opesial spines and one proximal spine. Scale bars: 12, 13, 14, 17 = 200 µm; 15, 16, 18 = 100 µm. A total of six paratypes , four from Station GeoB16375-1, one from Station GeoB16377-1, and one live colony on a coral from Station GeoB16388-3: Rosso-Bahama Collection Bah.H., PMC B 21. 30.6.2017 . Etymology. From the Latin, hirsutus , alluding to the prickly, thorny appearance of the frontal shield and the ooecium. Description. Colony encrusting unilaminar, pauciserial, small-sized, usually including few tens of zooids, sometimes more, irregularly elongated to ribbon-shaped ( Fig. 10 ), resulting from a single lobe or two lobes starting from the ancestrula and growing usually in opposite directions, sometimes bifurcating; lobes usually less than 1 mm wide and 1–5 mm long. FIGURES 19–25. Glabrilaria hirsuta Rosso n. sp. , Great Bahama Bank slope, all figures from Station GeoB16388-3, SMF- 45.513, except for 24 from Station GeoB16382-1, SMF-45.512. 19. Several ovicellate zooids with a more triangular frontal area of ectooecium and transversal crests with two central prominent spiny processes. 20. Close-up of the ooecium without a spiny crest, ooecium-bearing distal kenozooid is well seen. 21. Group of autozooids with very wide ooecia. 22. Periancestrular area. 23. Ancestrula with four oral spines bases and nine opesial spine bases (all articulated). 24. Ancestrula with the intramural budding. 25. Close-up of costae with prominent peripheral spiny processes, intercostal bridges and pores. Scale bars: 19, 22–24 = 200 µm; 20 = 100 µm; 21 = 500 µm; 25 = 50 µm. FIGURES 26–28. Glabrilaria hirsuta Rosso n. sp. , Great Bahama Bank slope. Orifices encircled by oral spine bases. 26. Orifice with six oral spines, Station GeoB16388-3, SMF-45.513. 27. Orifice with six oral spines, Station GeoB16368-1. 28. Orifice with seven oral spines, Station GeoB16368-1, SMF-45.507. Scale bars: 50 µm. FIGURES 29–38. Glabrilaria hirsuta Rosso n. sp. , Great Bahama Bank slope. 29. Kenozooids clustered within autozooids, Station GeoB16388-3, SMF-45.513. 30. Kenozooids marking the periphery of a lobe; note several pedunculate avicularia projecting above the substratum, Station GeoB16388-3, SMF-45.513. 31. Large kenozooid with extensive costate shields (arrowed), Station GeoB16367-2, SMF-45.506. 32. Group of small, particularly spiny kenozooids, GeoB16376-1, SMF- 45.509. 33. Very small irregularly-shaped kenozooids, some without a costate frontal shield, aligned between regenerated zooids, and possibly acting as reparative connections, GeoB16376-1, SMF-45.509. 34. Autozooid distally surrounded by kenozooids, GeoB16388-3, SMF-45.513. 35. Colony margin with ovicellate zooids, bounded by a series of kenozooids and a small reparative one located on the zooidal frontal surfacte (arrowed), several bearing pedunculate avicularia, GeoB16388-3, SMF-45.513. 36. Pair of pedunculate avicularia distal to an autozooid, Station GeoB16388-3, SMF-45.513. 37. Frontal view of pedunculate avicularium originating from a kenozooid, Station GeoB16388-3, SMF-45.513. 38. Damaged colony portion with teratologic zooidal morphology and including regenerated autozooids and kenozooids substituting autozooidal parts, Station GeoB16388-3, SMF-45.513. Scale bars: 29, 31, 33 = 500 µm; 30, 38 = 200 µm; 32, 34–36 = 100 µm; 37 = 50 µm. Zooids oval to roughly polygonal, small, longer than wide, moderately convex, distinct, the boundaries marked by deep furrows ( Figs 12–14 , 21 , 30–31 ); outlines irregularly sinuate. Gymnocyst narrow, deeply sloping towards the basal surface, 10–40 µm wide, but occasionally forming prominent tips, wedging between adjacent zooids, irrespective of their position ( Figs 22, 24 ). Communication in autozooids through c. 10 transversely oval windows of moderate size, positioned at the centre-line of distolateral walls ( Figs 12, 14, 15 ), c. six in kenozooids. Frontal shield subcircular to oval, occupying almost the entire frontal surface, formed by 14–18, but usually 16–17 wedgeshaped costae, converging towards the centre in the circular shields ( Fig. 13 ) or towards a median slightly raised carina in the oval shields ( Figs 11 , 15 ). Costae joined by 5–6 bridges leaving regularly spaced, oval to kidneyshaped intercostal pores about 8–10 µm wide ( Fig. 25 ), often bearing denticles, which mark the fusion of lateral processes. Only 3–4 intercostal pores are present proximally to the suboral pair of triangular costae that outline an almost right angle ( Figs 26–28 ). Suboral pair of costae stouter, merging at the midline and often forming a transversal crest of pointed, upward directed, spine-like processes nearly orthogonal to the frontal surface, and leaving two small round pores in the midline, one just proximal to the orifice and another on the opposite side of the transversal crest ( Figs 14 , 27, 28 ). Roundish papilla pores are seen between bases of costae, inside the peripheral intercostal pores. Costae with a median carina progressively raising towards zooidal margins, bearing up to four prominent, usually simple but sometimes bifid and even trifid, spine-like processes, the marginal ones, the longest, giving a concave appearance to the shield in heavily spinous zooids ( Figs 11 , 14 , 25 ). Spiny processes also mark the shield midline carina, when present ( Figs 19 , 29, 30, 38 ). Orifice transversally D-shaped ( Figs 12 , 20 , 26– 28 ), with the straight proximal border marked by an elevated rim and a curved distal one, slightly wider than long, provided with six articulated oral spines, seven on some periancestrular zooids and rarely also on adult zooids ( Fig. 28 ), long (50 µm) and slender, articulated on equally spaced bases, sometimes coalescing and forming a palisade distal to the orifice ( Fig. 36 ); four spines persisting on ovicellate zooids ( Figs 13–16 , 20 ), the distal ones abutting the proximal ooecium and slightly converging. Ovicells hyperstomial, cleithral. Ooecium formed by the distal kenozooid [ type 1 sensu Ostrovsky (1998 , 2008 , 2013 ) and type B sensu Bishop & Househam (1987) ], with 3–4 spiny costae, visible in frontal view ( Figs 13, 15, 16 , 35 ). Ectooecium with a usually barely visible longitudinal suture, but characterised by a planar semicircular to sub-triangular proximal area steeply inclined, bordered by aligned, pointed, spine-like processes directed distally and upwards, the central ones the most prominent, forming a transversal crest ( Figs 13–16 , 19– 21 ). A second crown of 3–6 spiny processes is situated distally, borne on the costate frontal shield of the kenozooid ( Figs 15, 16 ). Adventitious avicularia pedunculate, their cystid erect, from cone-shaped to elongated bell-shaped, with more or less narrow base, and variably directed, triangular rostrum, steeply inclined to the colony surface, and lacking pivotal denticles ( Figs 36, 37 ). Mandible triangular ( Fig. 37 ). Avicularia sparse, originating from basal porechambers on both autozooids and kenozooids (irrespective of the presence of an ovicell), often in clusters of 2–3 from adjacent pore-chambers ( Figs 35–37 ), easily detachable, and frequently lost, even in living colonies. Kenozooids very numerous, often more numerous than autozooids in certain colonies or colony portions, clustered together ( Fig. 29 ) or forming single ( Figs 12, 17 , 21 , 30 ) or double rows between autozooids, and commonly located along colony margins ( Fig. 10 ); more rarely interspersed between zooids ( Fig. 38 ). They are circular to polygonal in shape, often irregular, and, although variably sized, usually small in comparison to autozooids and less elevated. Kenozooids have extensive gymnocyst and a cribrimorph frontal shield of 4–7, usually six, costae in a radial pattern ( Figs 12, 17 , 19, 21 , 29–35 ); each costa bearing 1–2, sometimes three pointed, often very prominent spine-like processes ( Fig. 32 ). Large kenozooids with up to 10 costae have been occasionally found ( Fig. 31 ). Particularly small (less than 100 µm in maximum length), and irregularly shaped kenozooids with reduced, ill-defined or even lacking costate shield occur on broken zooids or are aligned in depressions between zooids in damaged colony portions ( Figs. 33, 34 ), clearly forming reparative patches. Ancestrula tatiform ( Figs 17, 18 , 22–24 ) bearing the bases of an unpaired proximal spine, and 5–6 pairs of spines borne around the edge of the gymnocyst; the two distal pairs around the opesia more closely spaced than the others. Ancestrula occupied by an intramural reparative kenozooid in all cases observed. The first zooid is budded from the ancestrula distolaterally; further budding typically continues just on one side of the ancestrula, and its lateral walls remain partly exposed ( Figs 17 , 22 ). Only one ancestrula was found being completely surrounded by zooids ( Fig. 24 ). Remarks. Glabrilaria hirsuta Rosso n. sp. significantly differs from other cribrimorphs and clearly falls within Glabrilaria as defined above. It is characterised by the small size of colonies and zooids, colony morphology, heavy spiny appearance of the colony surface, abundance and clustering of kenozooids, and ooecia with a transverse series of prominent processes. However, spine-like processes may develop at variable extent on zooids and especially on ooecia in different colonies. In some colonies and/or colony portions, ooecia even show only two very prominent median spiny processes. The ooecial outline could also vary from round ( Figs 13–16 ) or roughly triangular, about as long as wide, to irregularly quadrangular, wider than long ( Fig. 20 ). Ooecia may or may not be associated with stalked avicularia that are usually paired, and could be located near their proximal sides, borne on the maternal zooid ( Figs 13–16 ), or on their distal sides, borne on the associated kenozooid ( Fig. 21 ). Stalked avicularia may be apparently lacking in some colonies owing to their detachment, mostly in the central, oldest colony portions, and are usually particularly evident at colony margins because these areas correspond to the young, recently grown portions, and because there the avicularia stand up against the substratum background. Spiny processes and stalked avicularia may be hardly detectable on worn specimens, although they are extremely distinctive in live and well-preserved colonies. Intramural reparative regeneration was also very common in the studied material. Particular breakage of the frontal shields was also detected ( Figs 13, 14, 17 , 33 ) that can be, at least partly, interpreted as evidence of predation. In some instances, such broken zones are covered with small patches of frontal calcification ( Fig. 34 , arrowed). Also several orifices show inner (double and even third) rims ( Figs 12–16 ), pointing to the regeneration of certain zooids following predation (Berning 2008). These evidences indicate the heavy predation pressure on this species, and its difficult endeavour to protect itself notwithstanding the large number of oral spines and frontal spinous processes. Periancestrular astogenetic pattern is distinctive and leads to the development of elongated colonies where the ancestrula is located at one end of a single lobe or in between two ‘lateral’ lobes. In contrast, the ancestrula’s proximal budding loci seems to become active only late in astogeny. Several colonies in the present material were young and included a small number of zooids. Lobate pauciserial colonies are not uncommon in deep settings, although lobes tend to be fan-shaped rather than ribbon-like, and to develop distally to the ancestrula as in Herentia hyndmanni (Berning et al. 2008) and Atlantisina species ( Berning et al. 2017 ), among others. Within cribrilinids, Cribrilaria arrecta ( Bishop & Househam, 1987 ) n. comb. forms lobes with roughly unchanged width, which are, however, wider than in the present species. Cribrilaria arrecta n. comb. also shares with G. hirsuta Rosso n. sp. prominent carinate costae with pointed processes, but it significantly differs in several characters, among others in the large interzooidal avicularia with flabellate mandibles, a lower number of costae, and a different suboral bar. The zooidal spiny appearance of G. hirsuta Rosso n. sp. is reminiscent of specimens from the Kermadec region recorded as Puellina ( Cribrilaria ) innominata (Couch) by Gordon (1984, pl. 21, fig. C) , but other features, including the number of costae and oral spines, as well as the type of ovicell and avicularia, are completely different. Glabrilaria hirsuta Rosso n. sp. is clearly distinct from most species now allocated in Glabrilaria (see above), but resembles both G. pedunculata and G. cristata in its spinous colony surface, the common kenozooids, and the erect columnar avicularia. However, G. pedunculata has, among other characters, spot-like colonies, a relatively smooth appearance, and an ooecium with a prominent longitudinal carina (Harmelin 1988, figs 10, 11; Rosso et al . 2018 , fig. 5e, f). On the other hand, as stated by Harmelin (1978: 187) , and as it is evident from his images (fig. 7 and pl. 1, figs 8–10), G. cristata has more convex zooids with a shield of less numerous, yet more thorny, costae (ranging from a mean of 9.5 to 13 in colonies collected at 300 and 600 m depth, respectively), each bearing seven cristate spine-like processes converging in a sensibly raised carina; a suboral shelf including several intercostal spaces and only occasionally a single one; 4–5 costae in kenozooidal frontal shield; seven oral spines; a raised carina on the ooecium besides the spiny transversal one; and shorter zooids. However, the most distinctive character of G. cristata is the “peristomial” structure formed by the first pair of costae that elevate in a distally incomplete, denticulate collar that partly encircles oral spines. This structure is completely missing in G. hirsuta Rosso n. sp. Both G. cristata and G. hirsuta Rosso n. sp. occur in the shallow bathyal zone between 135–900 m ( Harmelin 1978 ) and 572–660 m depth interval (present data), respectively, and from temperate to subtropical latitudes at 29– 39° and 24–25° N, respectively. While G. hirsuta Rosso n. sp. is restricted to the western Atlantic, G. cristata occurs in central Atlantic seamounts and the Azores Archipelago. Glabilaria cristata is associated with the deepwater corals Madrepora oculata and Desmophyllum dianthus (two scleractinian coral species also reported from the Western Atlantic: see above), whereas G. hirsuta Rosso n. sp. was found preferentially on fragments of the dendrophylliid Enallopsammia profunda from coral rubble-rich sediments. In both Glabrilaria species the development of spiny processes on the costae and spiny projecting processes associated with the orifice and the ooecia, although differently shaped, could represent an adaptation for trying to cope with predation pressure in their habitats (see above). Both species are known exclusively based on present-day living populations and isolated dead specimens. Distribution. Glabrilaria hirsuta Rosso n. sp. is presently known only from the GBBS, with live colonies found at 572–660 m depth (see above), and dead specimens extending down to 677 m . Colonies were mostly found on erect branched corals, but encrusted also skeletons of other benthic invertebrates, including erect bryozoans, barnacle plates and the spicule net of the sponge Aphrocallistes . The finding of live specimens at station GeoB16388, where the occurrence of seepages is pointed out by lucinid associations ( Hebbeln et al. 2012 ), could indicate a certain environmental tolerance of this species.