Collarina gautieri Harmelin, 2019

Harmelin, Jean-Georges, Bishop, John D. D., Madurell, Teresa, Souto, Javier, Spencer Jones, Mary E. & Zabala, Mikel, 2019, Unexpected diversity of the genus Collarina Jullien, 1886 (Bryozoa, Cheilostomatida) in the NE Atlantic-Mediterranean region: new species and reappraisal of C. balzaci (Audouin, 1826) and C. fayalensis Harmelin, 1978, Zoosystema 41 (21), pp. 385-418 : 398-402

Collarina gautieri Harmelin , n. sp.

( Figs 8A; 9 ; 10 ; 11 ; 16A-D ; 17B ; 18D ; Tables 1-3 )

urn:lsid:zoobank.org:act:FB2B5A1F-6F84-426C-B460-69A6FB09E5B2

NE Atlantic, North Sea

Lepralia punctata – Busk 1854: 79-80 in part, pl. 96, fig. 3.

Cribrilina punctata var. a – Hincks 1880: 191, pl. 26, fig. 4.

Cribrilina punctata – Waters 1923: 563, figs 3, 7. — Echalier & Prenant 1951: 13. — Ryland & Stebbing 1971: 68, fig. 2b (top-right figure on p. 66; figures 1 and 2 are reversed relative to the legends on this page). — Hayward & Ryland 1979: 56, fig. 13. — Álvarez 1987: 44, pl. 9c-d.

Species A – Bishop 1986: fig. A.

Collarina balzaci – Bishop 1994: 242 (in part), figs 66-68. — Reverter et al. 1995: 125. — Reverter & Fernández 1996: 1248. — Hayward & Ryland 1998: 318 (in part), fig. 112a-b. — De Blauwe 2006: 126 (list); 2009: 270, figs 282-283; 2019: in press. — Souto et al. 2010: 1418 (list). — WoRMS image http://www.marinespecies.org/aphia. php?p=image&tid=110891&pic=23688 (accessed on 26.IV.2018).

Mediterranean

Cribrilina punctata – Calvet 1906: 398. — Prenant & Bobin 1966: 581 (in part). — Harmelin 1976: 227, 233, 236; 1977: 145; 1978b: 139. — Zabala 1986: 366, fig. 114.

? Collarina punctata – Gautier 1962: 108.

Collarina balzaci – Hayward & McKinney 2002: 37 (in part), figs 16a-c. — Chimenz Gusso et al. 2014: 154 (in part), figs 74c-d.

TYPE LOCALITY. — France, Marseille, Veyron.

TYPE MATERIAL. — Holotype. France, Marseille , Veyron, 43°12’44.2”N, 5°15’14.8”E, 23 m, 23.IX.1983, coll. by JGH, ovicelled colony of about 200 zooids, on fragmented empty Pinna nobilis shell, MNHN- IB-2014-1920.

Paratypes. France. 6 colonies including JGH stub 75, same origin as the holotype, on other shell fragments, MNHN-IB- 2014-1921. — Marseille, Morgiou Cape , 43°12’04.41”N, 5°27’08.22”E, 40 m, 20.I.1986, coll. by JGH, 3 colonies on empty Spatangus test,

MNHN-IB- 2014-1922. — Port-Cros Island, La Palud, 43°00’52”N, 6°23’26”E, 30 m, VI.1995, coll. by JGH, 1 colony on empty Pinna shell, SEM photos ( TM-MZ), MNHN-IB-2014 -1923.

OTHER MATERIAL EXAMINED. — Mediterranean. France. Marseille, Grand-Conglue Island , 43°10’33”N, 5°24’09”E, 62 m, 13.IX.1972, coll. by JGH, 6 colonies on pottery and glass fragments, MNHN . — Same origin as paratype 3, 1 detached colony . — Cassis , 20 m, 12.III.1971, 43°12’22”N, 5°30’44”E, coll. by JGH, 1 ovicelled colony on clay-pigeon target, MNHN . — Corsica, Bonifacio, R / V Travailleur 1881, Dr. 24, 55- 77 m, on shell: 1 colony labelled Cribrilina punctata, Calvet coll. ( Calvet 1906), MNHN-IB- 2008-2814 . — Corsica, Scandola, Elbu , 42°22’19”N, 8°33’21”E, 10 m, 30.VIII.2018, coll. by JGH coll., 2 colonies on small stones in cave, together with C. denticulata Harmelin , n. sp., MNHN, NHMUK . — Corsica, Scandola, Cala di l’Oru , 42°22’18”N, 8°32’42”E, 22 m, coll. by JGH, 2 colonies on stones, together with C. denticulata , MNHN . — Spain. Catalonia, Cap de Creus , 42°20’1.14”N, 3°17’10.09”E, 40 m, 17.VII.2017, on stone ( STUB 9121), coll. by TM-MZ, 1 colony, MZB . — Balearic Islands, Menorca Channel, 60 -80 m, VIII.2011, 39°51’01.5408”N,‰ 3°30’22.2948”E, on stone, INDEMAREScoll. by TM-MZ, 1 colony, MZB . — Catalonia, Medes Islands , 42°03’00.1332”N, 03°13’29.2512”E, 40 m, coll. by TM-MZ, one colony on stone, MZB . — Italy. Naples , NHMUK 1911.10 .1.684, SEM photos ( MSJ) .

NE Atlantic. France. Brittany, Roscoff, Taureau, G. Echalier dredging (depth unknown), 2.IX.1950, 2 colonies on Pecten shell, MNHN- IB-2014-446 . — W Brittany, R/V Jean-Charcot, 1968, DR01, 48°01’N, 05°44’W, 130 m, 3.XII.1968, B. Métivier leg. (= Bishop 1994, fig. 66), 1 colony on Chlamys shell, MNHN-IB-2008-13269. — Brittany, Roscoff, J.-L. d’Hondt leg., 1 colony on shell, MNHN- IB-2008-6553. — France, NHMUK 1911.10.1.686: Britain?, A. M. Norman leg., SEM photos ( MSJ) . — North Sea. Westhinderbank 2005, SEM photos (courtesy of H. De Blauwe ). — United Kingdom. Raasay Sound, Scotland, SEM photos ( JDB) (= fig. A in Bishop 1986 & fig. 67 in Bishop 1994), NHMUK 1973.4.6.1. — English Channel, Plymouth, off Stoke Point , 20-21 m, coll. by JDB, several colonies on bivalve shells and settled in culture tanks, NHMUK. — Spain. Galicia, Ria de Ferrol, 43°27’09”N, 08°18’51”W, 12 m, 13.IX.1989, dredging D-10 Reverter & Fernández (1996, as C. balzaci ), colony on shell, MHNUSC-Bry-126. — Galicia, Ria de Ferrol, 43°28’15”N, 08°15’30”W, 15 m, 13.IX.1989, dredging D-18 Reverter & Fernández (1996, as C. balzaci ), colony on shell MHNUSC-Bry-113. — Galicia, Malpica, 43°28’41’’N, 08°58’15’’W, depth unknown, 23.XI.2002, colony on echinoid test, SEM photos (courtesy of O. Reverter), MHNUSC-Bry-583. — Galicia, Cies Is., 42°12’41.38’’N, 08°54’20.37’’W, 12 m, 23.VIII.2012, on shell, SEM photos (courtesy of O. Reverter), MHNUSC-Bry-614. — Galicia, Ría de Vigo , several localities, 23-38 m, 1986, on shells, MHNUSC-Bry-34. — Galicia, Ría de Pontevedra , MHNUSC-Bry- 78j. — Portugal. S Portugal, Armaçao de Pêra Bay , 37°0’59.256”N, 08°11’25.367”W, 21 m, colony on calcareous algae and SEM photos MHNUSC-Bry-660. — S Portugal, Armaçao de Pêra Bay, 37°0’59.256”N, 08°11’25.367”W, 21 m, colony on calcareous algae and SEM photos, MHNUSC-Bry-661 .

ADDITIONAL RECORDS. — France, Brittany, off Roscoff , 90 m, 1 colony on Glycymeris shell, L. Cabioch dredging ( JGH leg.) . — Brittany, Pléneuf-Val-André, SEM photos (courtesy of H. De Blauwe) .

ETYMOLOGY. — Dedicated to the late Dr Y. V. Gautier, who contributed greatly to knowledge of the Mediterranean bryozoans.

DIAGNOSIS. — Colonies small- to medium-sized, early mature; autozooids with narrow marginal gymnocyst, costate shield composed of 7-12 costae bordered by a collar of large, prominent pelmata, one at the top of the steep base of each costa, pelmatidia often at the tip of a conical pillar; orifice with small L/W ratio; apertural bar with raised, massive umbo bearing 2 apical pelmatidia and 2 large basal pelmata; 3-5 oral spines; adventitious avicularia paired or single, directed laterally; ovicell frequent, associated with a pair of thick oral spines typically arched inwardly, ooecium kenozooidal, ectooecium bumpy, punctured with many pseudopores with prominent edge, the smaller at the tip of conical processes; ancestrula with 5 spines.

DESCRIPTION

Colony encrusting, pluriserial, unilaminar, small- to mediumsized (<500 zooids) ( Fig. 9A ). Autozooids more or less oval in outline. Gymnocyst narrow, little visible in frontal view, except for a short triangular proximal part ( Figs 9B, G ; 10B, C, E ). Costate shield subcircular to oval, with uneven surface ( Fig. 9C, F ); 7-12 costae, most frequently 9 (46%), with ascending base clearly defined, bearing a large, peripherally positioned pelma with a slightly prominent edge and funnel-shaped, i.e., with a large outer opening and a small inner pore; a smaller pelma, occasionally missing, in a more central position on the shield ( Figs 7G ; 8C, E). Intercostal lacunae relatively large, in most cases 3 more or less rectangular (Mediterranean) or 2 rounded (Atlantic) between adjacent costae ( Figs 9 ; 10 ). Apertural bar with a fairly high (particularly in ovicelled zooids), proximo-distally flattened umbo with proximal side slightly concave and large paired pelmata placed laterally at the base, tip often irregularly shaped but typically with two short pointed processes each with a sub-terminal lateral pelmatidium ( Figs 8A; 9C, D ; 10B, C). Sub-pedunculate avicularium inserted laterally to the apertural bar, paired or single, occasionally absent, directed laterally, tilted proximally at a shallow angle; proximal opesia large, rounded, with a narrow rim of cryptocyst; rostrum with a triangular mandible ( Figs 8A; 9B, D ); nested cystids occasionally present ( Fig. 17B ). Orifice of non-ovicelled zooids broader than long ( Table 1 ), poster straight with small lateral notches, anter semi-circular with each proximal end forming a slightly prominent triangular condyle ( Figs 8A; 9B ; 10E); orifice of ovicelled zooids clearly broader. Oral spines 3-5 in non-ovicelled zooids, in majority 4 (Mediterranean:> 70%, Atlantic:> 80%); in ovicelled zooids, two robust spines with basal parts particularly thick and long, typically bent toward the ovicell midline, and upper parts still relatively thick and curving back away from the ovicell midline ( Figs 9D, E ; 10B, C ). Ovicells frequent, apparently cleithral, ooecium hyperstomial, subspherical, formed by distal kenozooid at the colony border ( Figs 9E ; 10E ; 16 A- D); ectooecium with uneven surface owing to numerous large pelmata and pedunculate pelmatidia; an avicularium on the middle of the distal edge, distally directed, present in most cases (> 80%). Ancestrula cribrimorph with 5 spines, costate shield oval with 6-8 costae and gymnocyst clearly broader than in zooids of the zone of astogenetic repetition ( Figs 9H ; 10D, F ).

REMARKS

There are no marked morphological differences between Atlantic and Mediterranean specimens of C. gautieri Harmelin , n. sp. The only apparent divergence concerns the shape of intercostal lacunae that tends to be quadrangular in the Mediterranean and more rounded in the Atlantic, and their number, generally higher in the Mediterranean (three vs two). Throughout the Mediterranean and the NE Atlantic, specimens of this species were recorded either as Cribrilina punctata or Collarina balzaci . The taxonomic status of the latter was stabilized by Bishop (1988) with the designation of a neotype from the Mediterranean material examined by Waters (1879). At the same time, the confused background of records as C. punctata of the present species in the British Isles ( Busk 1854; Hincks 1880; Waters 1923; Ryland & Stebbing 1971; Hayward & Ryland 1979) was clarified by Bishop (1986, 1988, 1994). The species attribution of this northern material, however, was not clearly defined and the opinion of Bishop (1994) that it may belong to C. balzaci despite some morphological variations predominated afterwards. Examination of material or SEM photos corresponding to records of C. balzaci in the NE Atlantic ( Bishop 1994; Reverter et al. 1995; Reverter & Fernández 1996; Hayward & Ryland 1998; De Blauwe 2006, 2009, 2018; Souto et al. 2010) showed that these specimens presented all discriminant characters of C. gautieri Harmelin , n. sp. In the Mediterranean, the record of Collarina punctata at Marseille by Gautier (1962) was based on a few colonies encrusting shells and tests of echinoids in the 50 m depth zone, a habitat typical of C. gautieri Harmelin , n. sp., and on a specimen from Bonifacio (R/V Travailleur expedition) identified by Calvet (1906) as Cribrilina punctata . Examination of the latter, kept at the MNHN, confirmed conspecificity with the types of C. gautieri Harmelin , n. sp. The choice of Gautier (1962) to ascribe his material to the genus Collarina was appropriate and rather innovative, but did not involve Hassall’s species, particularly since he formerly considered that C. punctata was absent from the Mediterranean ( Gautier 1953), a statement also sustained by Bishop (1988, 1994) and Rosso & Di Martino (2016). This is also confirmed by the absence of Mediterranean specimens of true C. punctata in the material examined for this study. All Mediterranean specimens formerly recorded as C. punctata (e.g. Harmelin 1976; Zabala 1986) are, therefore, obvious misidentifications of Collarina and belong to C. gautieri Harmelin , n. sp., or to another Collarina species described here. Similarly, it is likely that the record without illustration of Cribrilina punctata from Tunisia ( Ben Ismaïl et al. 2007) corresponds to a Collarina species. Morphological features visible on several published SEM photos of Mediterranean specimens ascribed to C. balzaci are undoubtedly typical of C. gautieri Harmelin , n. sp., and this similarity is confirmed by their habitat: 1) specimen from northern Adriatic ( Hayward & McKinney 2002, Fig. 16 A-C), collected on sandy bottom at 30-40 m depth (site features supplied by L. Becniker, AMNH, pers. com., 24.X.2017); and 2) specimen from Palmorola Is., Tyr- rhenian Sea, Italy ( Chimenz Gusso et al. 2014: fig. 74c-d), collected at 88 m on detritic-biogenic bottom (site features supplied by C. Gusso, pers. com., 29.X.2017).

HABITAT AND GEOGRAPHICAL DISTRIBUTION

Unlike C. balzaci , all specimens of C. gautieri Harmelin , n. sp. collected in the NE Atlantic and the Mediterranean were not epiphytic but occupied the same alternative type of habitat, i.e., small substrates, mainly shells, on coarse sandy bottom ( Fig. 18D ). The depth range of these samples was broad in the Atlantic, from the intertidal zone (Ria de Ferrol: Reverter & Fernández 1996) to 130 m (W Brittany: specimen MNHN-IB-2008-13269). The “Faciès à Cribrilina punctata ” recorded by Prenant (1927) on stones in hollows of the upper intertidal zone at Roscoff (Brittany) may correspond to a particular abundance of C. gautieri Harmelin , n. sp. An experiment of small-scale cultivation of a different shell-encrusting species in Plymouth at the laboratory of the Marine Biological Association revealed an unexpected spontaneous settlement of C. gautieri Harmelin , n. sp. with the development of circular colonies. The very high proportion of ovicelled zooids in these colonies suggests that this species has large adaptive capacities to colonize opportunistically available substrata in the Atlantic coastal zone. In the Mediterranean, the habitat niche of this species is narrower as shown by the collected material, in any case found on shells, stones or pottery fragments in contact with coarse soft bottom, at depth ranging from 10 m to 88 m. The geographical distribution of C. gautieri Harmelin , n. sp. covers both the NE Atlantic and the Mediterranean. In the Atlantic, it is widely distributed from the Faeroes and the Shetlands ( Bishop 1994) to the southern coasts of the Iberian Peninsula. In the Mediterranean, its range is seemingly more limited, perhaps owing to sampling bias induced by less-extensive habitat in this sea (see below) ( Fig. 11 ).

Figures

FIG. 1. — Savigny’s drawings (1817: pl. 9). Flustra balzaci Audouin, 1826, in Savigny’s figure 8, and Flustra jauberti Audouin, 1826, in Savigny’s figure 9.

FIG. 10. — Collarina gautieri Harmelin, n. sp., NE Atlantic:A, Lepralia punctata Hassall, 1841: Busk 1854, pl. 96, fig. 3; B, C, ovicelled and non-ovicelled autozooids, note the typically curved spines associated with ovicells, the orientation of the avicularia and the respective extent of costate shield and gymnocyst; D, part of a young colony including the ancestrula (right) and the colony edge with 2 ovicelled zooids (left); E, non-ovicelled zooid (right) and fertile zooid with an early stage of the ooecium formation (middle), note the typical shape of the orifices and the structure of the costate shield with large marginal pelmata; F, ancestrula. Origin: B, Devon, coll. by JDB; C, NHMUK 1973.4.6.1, Raasay Sound, Scotland: Species A, Bishop (1986); D, Galicia, Malpica; E, Galicia, Ferrol; F, Algarve, coll. by JS. Scale bars: B, D, 200 µm; E, F, 100 µm.

FIG. 11. — Geographical distribution of Collarina gautieri Harmelin,n. sp. in the NE Atlantic and the Mediterranean.Origin of records:Red, Atlantic;1-5, Bishop (1994); 6, De Blauwe (2006); 7-8, MNHN; 9, De Blauwe (2019); 10, Álvarez (1987); 11-12, Reverter collection;13, Souto et al.(2010);Blue, Mediterranean; 1-2, this paper, coll. by TM-MZ; 3-4, this paper, coll. by JGH; 5, MNHN collection, Calvet (1906); 6, Chimenz Gusso et al. (2014); 7, NHMUK 1911.10.1.684; 8, Hayward & McKinney (2002).

FIG. 16. — Phases of ooecium construction involving a daughter zooid (kenozooid or autozooid) of the maternal zooid in Collarina Jullien,1886 species:A-D, growth of entooecium with bilobate stages, and its incorporation by distal kenozooid in C. gautieri Harmelin, n. sp.; E, ooecium formed by a distal autozooid in Collarina denticulata Harmelin, n. sp., three successive early stages (1, 2, 3: SEM photo + stylized outlines) at the colony edge from single to bilobate blade with unequal lobes, and three older stages (I, II, III) with distal autozooids incorporating progressively the growing entooecium. Origin: A-C, Marseille, Veyron; D, S Portugal, MHNUSC-Bry-661; E, Medes Islands, on Pinna shell. Scale bars: B-D 100 µm; E, 200 µm.

FIG. 17. — Adventitious avicularia with nested cystids in Collarina Jullien, 1886 species: A, C. macaronensis Harmelin, n. sp., ovicelled zooid; B, C. gautieri Harmelin, n. sp., four piles of nested avicularian cystids adventitious on two autozooids and an ooecium; C, C. macaronensis Harmelin, n. sp.; D, C. fayalensis Harmelin, 1978; E, C. speluncola Harmelin, n. sp. Origin: A, Madeira, NHMUK 1899.7.1.2105; B, Galicia, Ria de Ferrol, MHNUSC-Bry-113; C, Galicia, Sisargas Is., MHNUSC-Bry-662; D, Azores, Saô Miguel, Vila Franca; E, Marseille, Conger Cave. Scale bar: A, 100 µm.

FIG. 18. — Habitats of Collarina species:A, C. balzaci (Audouin,1826), bundles of Posidonia leaves; B, C. speluncola Harmelin,n. sp., wall of dark submarine cave with freshwater seepage; C, C. denticulata Harmelin, n. sp., underside of pottery fragment, Cassis, Port-Miou, 18 m; D, C. gautieri Harmelin, n. sp., underside of Pinna shell, paratype MNHN-IB-2014-1921, Veyron, 24 m; E, C. macaronensis Harmelin, n. sp., underside of pebble, paratype MNHN-IB-2014-1926, Madeira, Porto Santo, Baixo Is.; F, C. fayalensis Harmelin, 1978, underside of pebble, Azores, Saô Miguel, Vila Franca, 15 m. Scale bars: 1 cm.

FIG. 7. — Outlines of orifice,apertural bar,avicularium and portion of costate shield and gymnocyst:A, Collarina balzaci (Audouin,1826);B, C. fayalensis Harmelin, 1978, C, C. denticulata Harmelin, n. sp. Scale bar: 100 µm (orifices), 50 µm (avicularia).