On some “ Hemicyclopora ” Norman, 1894 and “ Escharella ” Gray, 1848 species (Bryozoa, Cheilostomatida) from the Atlantic-Mediterranean region. Re-examination of their generic status and description of new species and a new genus Author Harmelin, Jean-Georges Station marine d’Endoume (SME), Observatoire des Sciences de l’Univers (OSU) Pytheas, Institut méditerranéen d’Océanologie (MIO), Groupement d’Intérêt scientifique (GIS) Posidonie, Aix-Marseille University, F- 13007 Marseille (France) jean-georges. harmelin @ univ-amu. fr / jg. harmelin @ gmail. com harmelin@gmail.com Author Rosso, Antonietta Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Università di Catania, Corso Italia 57, I- 95129, Catania (Italy) and Consorzio Interuniversitario per le Scienze del Mare (CoNISMa), Piazzale Flaminio, 9, I- 00196, Roma (Italy) rosso @ unict. it rosso@unict.it text Zoosystema 2023 2023-06-15 45 10 373 407 journal article 10.5252/zoosystema2023v45a10 1638-9387 8056122 urn:lsid:zoobank.org:pub:370E4D0A-FF10-4CAC-AF9F-A1A866FC1BEB Hemicyclopora hexaspinae n. sp. ( Figs 10 D-F; 11A-G; 12A-E; Tables 1 ; 2 ; 4 ) urn:lsid:zoobank.org:act: E749E551-2748-4D15-BD80-A92CB661B657 Hemicyclopora discrepans – Harmelin 1997: 144 , table 2. Hemicyclopora multispinata – Di Geronimo et al. 1990 : table 1. TYPE LOCALITY . — France , La Ciotat, 3PP Cave. TYPE MATERIAL . — Holotype . Mediterranean, France • 1 colony, c. 20 zooids (5 ovicells) + ancestrula; La Ciotat , 3PP Cave, 25 m depth from entrance; 73°09’47.9”N , 5°35’59.8”E ; 20 m depth ; 15.I.1993 ; Div.; JGH leg.; MNHN-IB-2017-771 . Paratypes . Mediterranean , France • 1 coated colony, c. 23 autozooids (4 ovicells); La Ciotat , 3 PP Cave , 40 m from entrance; 73°09’47.9”N , 5°35’59.8”E ; 21 m depth ; 28.XI.1991 ; Div.; JGH leg.; MNHN-IB-2017-772 • 1 coated colony, c. 30 autozooids (1 ovicell); Marseille , ‘ Calanques’ Coast , Cape Morgiou Cave ; 73°12’05.8”N , 05°27’08.11”E ; 27 m depth ; 26.IX.1967 ; Div.; JGH leg.; MNHN-IB-2017-773 . Italy • 1 ovicellate colony with ancestrula; Ustica Island , Apollo Bank ; c. 38°7’N , 13°1’E ; 60 m depth ; VI.1986 ; Dre; AR leg.; PMC . B32.12.12.2020 . OTHER MATERIAL EXAMINED . — Mediterranean , France • 1 colony; Marseilles , ‘ Calanques’ Coast , Eissadon Cave ; 73°12’07”N , 5°29’24.2”E ; 5 m depth ; 17. VI .1992 ; Div. ; JGH leg.; MNHN • c. 13 colonies (12 sampled spots); La Ciotat , 3PP Cave ; 19-25 m depth ; same site as for holotype ; from XI.1991 to XI.1994 ; Div. ; JGH leg.; MNHN . Italy • 7 colonies + fragments; S Tyrrhenian Sea , Ustica Island , Apollo Bank, same data as for paratype PMC. B32.12.12.2020; PMC Rosso-Collection I. H. B. 91a • 4 colonies; W Ionian Sea, SE Sicily , Catania , off Acitrezza Marine Protected Area , 110 m depth (2 col.); Ciclopi survey; VII.2000 ; Stn 8I; 95 m depth (1 col.) & Stn 9G; 63 m depth (1 col.); coarse DC with Würmian biogenic remains; Dre; AR leg.; PMC Rosso-Collection I. H. B. 91b. Atlantic Ocean, western approach of Gibraltar Strait • 1 small colony on shell; R / V Cryos ; Balgim Expedition ; Stn DR 42; 35°54.5’N , 6°13.3’W ; 133-137 m depth ; 2. VI .1984 ; Dre ; JGH leg.; MNHN • 2 small colonies; R / V Cryos ; Balgim Expedition ; Stn DW 43; 35°54.1’N , 6°14.5’W ; 150 m depth ; 2. VI .1984 ; Dre ; JGH leg.; MNHN • 1 small colony on shell; R / V Cryos , Balgim Expedition ; Stn DR 49; 35°53.0’N , 6°32.8’W ; 518-524 m depth ; MNHN . ETYMOLOGY. — From Latin hexa (six) and spinae (spines), in apposition, for the typical number of oral spines of this species in both ovicellate and non-ovicellate autozooids. DIAGNOSIS . — Autozooids bulged, frontal shield finely granular with usually small to medium-sized marginal pores. Orifice terminal, condyles prominent with blunt tips, proximal edge more or less concave, without suboral umbo. Oral spines six in both non-ovicellate and ovicellate autozooids with the proximal pair arched inwardly and the distal ones outwardly. Ovicell presumably semicleithral, attached to the distal wall of the maternal zooid, produced by a small, basal kenozooid, narrower than autozooids; endooecium finely granular, without proximal thickening. Ancestrula with an extended cryptocyst and a narrow proximal gymnocyst, and 10-11 spines, four of them edging the cryptocyst. DESCRIPTION Colony encrusting, unilaminar, small (in most cases, less than 30 zooids). Autozooids relatively small ( Table 1 ), longer than wide (L/W: 1.31), relatively poorly calcified, cystid with maximum thickness at orifice level; frontal shield markedly bulging, finely granular ( Figs 11A, D ; 12B ); marginal pores very small and poorly visible in specimens from caves (about 5-7 µm; Fig. 11 A-C) or larger in colonies from open soft bottoms (20-25 µm; Figs 11D, E ; 12B ); disto-lateral and distal walls subvertical, with numerous small basal pore chambers ( Fig. 11 A-D). Orifice distal, slightly broader than long; proximal edge (= poster) slightly concave or nearly straight, without proximal umbo or thickened rim; condyles triangular, slightly curved proximally, located just above the poster corners ( Figs 10D, E ; 11A, F ). Six oral spines in both non-ovicellate and ovicellate autozooids, exceptionally seven in non-ovicellate zooids (about 2% in available samples from Mediterranean caves), relatively short, with an open tip, articulated on thick, barrel-shaped bases ( Figs 10D ; 11 E- G); in both non-ovicellate and ovicellate zooids, spines of the proximal pair arched inwardly while spines of the distal pair arched outwardly ( Fig. 11 A-G). Ovicells kenozooidal, present at the colony margin ( Fig. 11 A-E), attached to the distal wall of the maternal zooid and on a tiny kenozooidal base, ovoid, significantly narrower than the maximum width of the maternal autozooid, presumably semicleithral ( Fig. 11C ); endooecium finely granular, imperforate, a small, triangular labellum sporadically present, with smooth surface suggesting a gymnocystal origin (outer fold of the ooecium floor?). Ancestrula with typical structure, opesia with a concave proximal border rimmed by a narrow band of smooth calcification, cryptocyst particularly extensive, and gymnocyst wide laterally but drastically narrowing proximally, four spines bordering the distal half of the cryptocyst and six, exceptionally seven, opesial spines; one autozooid budded distally ( Figs 10F ; 12B, D ). The ancestrula or an autozooid can occasionally produce a tubule from a lateral pore chamber, at the extremity of which an autozooid may be budded ( Fig. 12 C-E). FIG . 10. — Distal part of ovicellate and non-ovicellate zooids, and ancestrulae,all at the same scale: A -C , Hemicyclopora neatonensis n. sp. ; D -F , H. hexaspinae n. sp. ; G - I , Escharella similis Ramalho, Rodríguez-Aporta & Gofas, 2022 . Drawings from SEM pictures and examination under stereomicroscope. Origin: A -C , Sicily; D -F , Provence; G -I , Alboran Sea. Scale bar: 200 µm. REMARKS Morphological features The most obvious distinctive features of H. hexaspinae n. sp. are: 1) the number of oral spines, six in both ovicellate and non-ovicellate zooids, which are articulated on particularly large, barrel-shaped bases; 2) the distinctly terminal orifice, with a strait or slightly concave proximal edge, without a proximal umbo; 3) the very convex frontal shield of autozooids; 4) the downcurved, triangular shape of the condyles; 5) the comparably small, nearly isodiametrical ovicells produced by a tiny basal kenozooid; and 6) the ancestrula with a broad cryptocyst and a very narrow proximal gymnocyst. The small size of colonies with a high frequency of ovicells and the predominantly peripheral position of the latter are also typical. Samples from the large, dark 3PP cave attest to these features: the number of autozooids of 17 collected colonies ranged from three to 30 (mean = 13 ± 6 AZ, but many zoecia were empty), with a high proportion of ovicellate ones (71%). The occurrence of ovicells is predominant at the colony margin (74%). This peripheral location may indicate a growth stop of the colony due to insufficient energy allocation after reproduction, a condition observed in dark caves when food inputs are sporadic ( Harmelin 1997 ). Specimens from soft bottoms in the open sea differ from those from dark caves essentially in the larger size of their marginal pores. This difference might be related to the dynamics of growth in these two environments, which is very slow in dark caves with poor exchanges with the open sea ( Harmelin 2000 , see below). The semicleithral type of the ovicell closure was identified by A. Ostrovsky (personal communication to JGH , 18.X.2022 ) from a SEM picture ( Fig. 11C ) showing an ovicell partially closed by the ooecial vesicule and a sclerite. FIG . 11. — Hemicyclopora hexaspinae n. sp. : A , ovicellate and non-ovicellate zooids at the edge of a small colony, with frontal shield bulged and granular; B , C , ovicellate zooids: terminal ovicells with six curved spines, attached to maternal distal wall and lying on a small kenozooid responsible for ovicell formation; D , colony edge with six ovicells: two fully grown and four under construction from a basal kenozooid; E , ovicellate zooid with thick bases of spines; F , orifice of non-ovicellate zooid: six basal parts of spines, concave proximal edge and prominent condyles; G , shape of the oral spines in a non-ovicellate zooid:. Origin: A , B , F , G , paratype MNHN-IB-2017-772, Provence, 3PP Cave; C , paratype MNHN-IB-2017-773, Provence, Cape Morgiou Cave; D , paratype PMC.B29.8.11.2020; Ustica Is., Apollo Bank; E , Atlantic, Balgim DR49. Scale bars: A, D, 300 µm; B, E, G, 100 µm; C, 200 µm; F, 50 µm. FIG . 12. — Hemicyclopora hexaspinae n. sp. : A , ancestrula, note the large size of the cryptocyst; B , ancestrula and daughter zooids; C , autozooid with a tubule budded from a distolateral pore-chamber; D , ancestrula with three successive daughter zooids, the third one with a basal tubular part budded by the ancestrula; E , same ancestrula and zooids, sketch from stereomicroscopic examination: darkening by Mn-Fe oxides increasing from the youngest zooid to the ancestrula attesting to the very slow growth in confined dark caves. Origin: A , C -E , Provence, 3PP Cave; B , Ustica Island, Apollo Bank. Scale bars: A, 50 µm; B, 300 µm; C-E, 100 µm. Taxonomic issues Hemicyclopora hexaspinae n. sp. differs from Mediterranean congeners particularly in the number of oral spines, shape of the orifice, and type of ovicells ( Table 2 ). This species has several characters in common with H. discrepans ( Table 2 ): a bulged frontal shield with a granular texture, absence of a thickening or umbo proximally to the orifice and on the ovicell, protuberant triangular condyles, poster concave or straight, oral spines with very thick bases, distal wall subvertical, ovicell apparently terminal but associated with a small basal kenozooid. However, H. hexaspinae n. sp. differs clearly from H. discrepans in having constantly six spines instead of eight in non-ovicellate zooids, and an ancestrula with the proximal gymnocyst poorly developed and the cryptocyst area widely extended proximally ( Figs 10F ; 12A ). Among other Recent Hemicyclopora species , the boreal H. emucronata ( Smitt, 1872 ) , also has six oral spines in both ovicellate and non-ovicellate zooids ( Smitt 1872 : fig. 27; Kluge 1962 : fig. 270). However, available SEM pictures of Smitt’s type and of a specimen from Spitsbergen (Kuklinski et al. , website Atlas of Arctic Bryozoa , accessed on 30. IX .2020 ) show that H. emucronata clearly differs from H. hexaspinae n. sp. The former has zooids with a flatter frontal shield, the ovicell endooecium is continuous with the frontal shield of the distal zooid, and the ancestrula has a different structure. HABITAT DISTRIBUTION The available material of H. hexaspinae n. sp. was collected in two habitats which are quite opposite in terms of environmental conditions and type of substrates: walls of dark parts of shallow submarine caves vs biogenic remains at the surface of relatively deep soft bottoms ( 60-150 m ) in the open sea. In underwater caves from the Marseille area, H. hexaspinae n. sp. was present with tiny, frequently ovicellate colonies (“spot colonies”, Bishop 1989 ; Okamura et al. 2001 ). However, in dark caves with low energy inputs from the outside, the occurrence of ovicells in tiny colonies is not a sign of early fertility and high offspring production, such as in r-selected species (e.g. Pianka 1970 ) from productive environments. On the contrary, in dark caves, the growth of bryozoan colonies is limited to a very low yearly production of zooids. This feature is revealed by the external aspect of zooids, which are more or less blackened by deposits of Mn and Fe oxides that increase over time ( Allouc & Harmelin 2001 ), a common phenomenon in aphotic habitats. This is exemplified by a tiny colony from 3PP Cave composed of the ancestrula and three autozooids ( Fig. 12D, E ), each budded very sporadically as shown by the increasing darkening of the frontal wall and spines from the third, youngest, zooid to the ancestrula. Such populations and colony features are signs of an adaptive strategy for life in highly cryptic and oligotrophic habitats where energy inputs from the outside are very limited and sporadic ( Harmelin 2000 ; Okamura et al. 2001 ). Another peculiarity of the occurrence of H. hexaspinae n. sp. in cryptic habitat is its uneven distribution among caves clustered in the same area. Along the coast from Marseille to La Ciotat, despite the great frequency of this habitat (mostly karstic cavities), specimens were recorded in only three caves. Most of them were collected in the vast 3PP Cave, but none in the similarly large Trémies Cave, close to the former (linear distance: < 8 km ), despite extensive sampling of its dark parts (e.g. Harmelin 1969 , 1986 ). Differences in the inner thermal regime of these two caves might be the cause of this uneven distribution. In 3PP Cave, because of a descending profile ( Harmelin 1997 ), yearly fluctuations are reduced (12.8- 14.5°C) and close to those of the homothermic deep-sea. In contrast, in the Trémies Cave, due to a karstic origin, the inner ascending profile leads to the trapping of warm water bodies in the upper dark parts ( Harmelin 1969 ). However, H. hexaspinae n. sp. was also present in two other shallow caves (Cape Morgiou, Eissadon) where the inner thermal regime fluctuates as in the open sea at the same depth. The punctuated distribution of H. hexaspinae n. sp. in caves of the Provence region suggests that connectivity between caves is very low and recruitment is mostly autochthonous. In the same region, H. hexaspinae n. sp. was never recorded in deep-water samples ( 100-300 m , rock fragments, dead shells, coral skeletons) from the shelf and the neighbouring Cassidaigne Canyon (Harmelin 1976, table III and unpublished data). In southern Italy , small living and dead colonies of H. hexaspinae n. sp. were found on the outer shelf, in thanatocoenoses occurring at the surface of detritic biogenic bottoms (Ionian Sea, eastern Sicily ), and also at the top of the Apollo Bank where rocky outcrops with Laminaria rodriguezii Bornet, 1888 alternate with coarse detritic sand. Living colonies were mostly colonising small rhodoliths, fragments of coralline algae, dead branches of erect bryozoans [e.g. Adeonella calveti Canu & Bassler, 1930 and Smittina cervicornis (Pallas, 1766) ] and shells. GEOGRAPHICAL DISTRIBUTION Obviously, the small size of colonies of H. hexaspinae n. sp. , the types of substrates on which they grow, and their scattered condition increase considerably the stochasticity of records. Therefore, its actual geographical distribution is poorly known. Most records were from the western Mediterranean Sea, in Provence, in the southern Tyrrhenian Sea, and in the western Ionian Sea (Sicily). This species has also been collected in the NE Atlantic, close to the western entrance of the Gibraltar Strait ( Table 4 ). This occurrence in the Gulf of Cadiz, down to 524 m depth, may suggest a possible influence of the Mediterranean outflow water (e.g. Bashmachnikov et al. 2015 ) on the composition of the bottom fauna.