Taxonomic remarks on Bela atlantidea (Mollusca: Gastropoda: Mangeliidae) and updated distribution in the Mediterranean basin

Marine Biodiversity Records, page 1 of 6. # Marine Biological Association of the United Kingdom, 2012 doi:10.1017/s1755267212001091; Vol. 5; e120; 2012 Published online Taxonomic remarks on Bela atlantidea (Mollusca: Gastropoda: Mangeliidae) and updated distribution in the Mediterranean basin paolo mariottini 1, carlo smriglio 1, sergio calascibetta 2 and andrea di giulio 1 1 Dipartimento di Biologia, Università Roma Tre, Viale Guglielmo Marconi 446, 00146 Rome, Italy, 2 Via F. Domenico Guerrazzi 53, 90135 Palermo, Italy Brachycythara atlantidea (Knudsen, 1952) and B. beatriceae Mariottini, 2007, both species belonging to the family Mangeliidae, are here moved to the genus Bela Gray, 1847, based on morphological shell features. The new epithets are: Bela atlantidea (Knudsen, 1952) comb. nov. and Bela beatriceae (Mariottini, 2007) comb. nov. The recently described Bela clarae Peňas & Rolán, 2008 is here considered a junior synonym of B. atlantidea according to a comparative scanning electron microscopy analysis of the shells. The distribution of B. atlantidea in the Mediterranean basin is therefore reconsidered including all known records of B. clarae. Keywords: Brachycythara atlantidea, Brachycythara beatriceae, Bela clarae, taxonomy, Mediterranean Sea Submitted 21 March 2012; accepted 5 November 2012 INTRODUCTION The genus Brachycythara Woodring, 1928 has been re-described by Powell (1966) and comprises small Recent and Tertiary turrids that mostly occur in the Caribbean area. The type species of this genus, Cythara gibba Guppy, 1896, comes from the Oligocene of Jamaica (Guppy & Dall, 1896: p. 306, plate XXVII, figure 9) and was recombined by Woodring (1928) as Brachycythara gibba (type specimen USNM 107144). The taxon Cythara atlantidea Knudsen, 1952 was described on two shells collected during the Danish Expedition to the Coasts of Tropical West Africa, 1945 1946. The type locality of this species is at coordinates 10822 N 016822 W (Guinea) (Knudsen, 1952: p. 172); its distribution in the eastern Atlantic Ocean has been subsequently enlarged, ranging from Senegal to Angola, by the report of Rolán & Otero-Schmitt (1999: p. 21), who ascribed the species to the genus Brachycythara. Thereafter, B. atlantidea has been reported from the southern coast of Spain (Costa del Sol, Alboran Sea) by Smriglio et al. (2007). It was proposed that the Mediterranean shells of B. atlantidea were representatives of a pseudopopulation (sensu Bouchet & Taviani, 1992), derived from passively drifting larvae from the nearby Atlantic Ocean. The multispiral protoconch of this species (indicative of planktotrophic larval development) supports this hypothesis. Recently, a fresh specimen of this turrid has been found in Sicily, which is the first record of the species from the Italian coast. Corresponding author: P. Mariottini Email: mariotpa@uniroma3.it In the present paper we compare B. atlantidea with the closest species, B. beatriceae (Mariottini, 2007) and B. clarae Peñas & Rolán, 2008 (in Peñas et al., 2008), reviewing their taxonomic status, and updating their distribution in the Mediterranean basin. Abbreviations used: Ex, exx, specimen, specimens; MNHN, Muséum National d Histoire Naturelle, Paris, France; MZB, Museo di Zoologia dell Università di Bologna, Bologna, Italy; USNM, United States National Museum of Natural History, Washington, DC, USA; ZMUC, Zoologisk Museum, Copenhagen, Denmark. MATERIAL EXAMINED The following specimens of Bela atlantidea were examined: 1 ex was trawled off Carini, Palermo, Sicily (38814 N 013811 E), trawled at 75 m depth by the fishing net of the vessel Annagaia ; 3 exx off Estepona (36825 N 5809 W), Spain, trawled at 150 250 m depth; 1 ex off Adra (36845 N 3801 W), Spain, trawled at 80 150 m depth; 2 exx off Malaga (36833 N4822 W), Spain, trawled at 50 m depth; 2 exx off Marbella (36828 N4852 W), Spain, trawled at 30 40 m depth; 2 exx from the coast of West Sahara, trawled at 30 60 m depth. All specimens, with the exception of the Sicilian record, were previously cited in Smriglio et al. (2007). The paratype MNHN-21396 of B. clarae was examined both by light microscopy and scanning electron microscopy (SEM). SEM photographs were taken at the Interdepartmental Laboratory of Electron Microscopy (LIME), Università Roma Tre, Rome, Italy. Current 1

2 paolo mariottini et al. systematics is based on the classification proposed by Bouchet et al. (2011). TAXONOMY Class GASTROPODA Cuvier, 1795 Family MANGELIIDAE P. Fischer, 1883 Genus Bela Gray, 1847 Type species (by subsequent designation) Murex nebula Montagu, 1803 Genus Brachycythara Woodring, 1928 Type species (by original designation) Cythara gibba Guppy, 1896 Bela atlantidea (Knudsen, 1952) comb. nov. Cythara atlantidea, Knudsen 1952, Videnskabelige Meddelelser fra Dansk naturhistorisk Forening I Kjobenhavn 114, 172 173, plate III, figure 5; Brachycythara atlantidea, Rolán & Otero-Schmitt 1999, Argonauta 1, 21, figures 73 78. original description Shell turriform with a fairly low spire. About 8 whorls are present separated by a suture, which is not very deep. The protoconch consists of about 2 1 / 2 whorls completely without sculpture. The upper part of the adult shell is ornamented with faint close set ribs, which gradually become more distant and prominent. On the body whorl and to a lesser degree on the penultimate whorl the ribs are slightly flexuous across the subsutural band, being at the same time broader and less distinct. On the body whorl 10 ribs are present. A spiral sculpture consisting of 2 3 lines is seen on the uppermost part of the adult shell. The number of striae is gradually increased, they are most distinct across the ribs, but are also seen in the interstices between these. On the body whorl about 30 spiral lines are present, while 8 9 are seen on the penultimate whorl. Besides this spiral sculpture a very delicate granulose sculpture can be detected under the microscope. The sculpture is found all over the adult shell and consists of regular rows of rounded granules. On the subsutural band they are arranged in curved axial rows. On the remaining part of the whorl they are present only in the interstices between the spiral lines. They are here arranged in spiral rows of which two or three are found in each interstice. Aperture oblong. Columella slightly convex. Outer lip simple, convex. Sinus broad. Sipho short and very broad. Coloration: greyish white becoming faintly brownish towards the upper whorls. Measurements: Holotype: 7.3 3.0. Paratype: 6.0 2.6. type locality and type material Guinea, 10822 N 016822 W, 41 55 m depth. Holotype and paratype in ZMUC. distribution Eastern Atlantic Ocean, from Senegal to Angola, Mediterranean Sea. italian record of bela atlantidea A specimen of B. atlantidea was collected from Sicily (Figures 1A 8) and compared to other material collected from the Atlantic Ocean and the Alboran Sea (Figure 9 and see MATERIAL EXAMINED) and it was unequivocally identified by means of SEM photographs. Bela beatriceae (Mariottini, 2007) comb. nov. Brachycythara beatriceae, Mariottini 2007, Nautilus 121,159 162, figures 1 9, 13 20. original description Shell rather small, to 10.9 mm in length, holotype 8.6 3.4 mm, biconical, elongate fusiform, solid, spire about half total height. Protoconch multispiral, dome shaped, of 3 3.5 strongly convex whorls, first 1.5 2 whorls smooth, remainder reticulated being composed of oblique axial costae crossed by spiral ribs of about equal width; protoconch indicative of a planktotrophic larval development. Diameter of protoconch about 700 750 mm. The protoconch teleoconch transition not well marked. Teleoconch of 5 6 whorls, weakly angulate near middle of spire, sutural ramp gently concave, whorl sides gently convex; last whorl about 2/3 shell length. Axial sculpture consisting of 7 8 prominent, slightly opisthocline, flexuous, and narrowly rounded axial folds; folds regularly spaced, with much broader interspaces, reaching from suture to suture on spire but fading out after crossing the shoulder slope and at about the middle of the base. Spiral sculpture of numerous very fine threads that densely alternate with bigger interspaces; the subsutural thread shows well-marked axial denticles. At higher magnification, it can be observed that each interspace consists of several (up to five) rows of rounded tiny granules, each one linked axially to the upper and lower thread by a very fine connection. Aperture narrow, ovate, about one-third of the shell height. Siphonal canal short, narrow, and open. Inner lip with a moderately developed parietal callus pad. Outer lip thin or variced, according to the stage of growth, whether the lip coincides with an axial rib or an interspace. Anal sinus marked, arcuate on shoulder slope. Shell color white, with a brown band on lower half of body whorl (juvenile and subadult shells uniformly white); a darker spot present on the outer lip at the boundary of the white and the brown colors. type locality and type material Alboran Sea, Spain, off Marbella, 36828 N4852 W, 30 40 m depth. Holotype No. 31032 in MZB. distribution Alboran Sea (Costa del Sol, Spain) and eastern Atlantic Ocean (West Sahara). bela clarae type material The paratype MNHN-21396 of Bela clarae (Figures 10 16) was analysed by light microscopy and SEM and the examination of its protoconch, consisting of 3 whorls, revealed a bigger diameter (650 mm) than the one reported for the holotype (476 mm). The general shell feature of this paratype (protoconch and teleoconch sculpture, 9 teleoconch axial folds of the last whorls, teleoconch length/width ratio of 2.4, shell colour uniformly yellowish-brown) are perfectly matching the ones re-described for B. atlantidea in Mariottini (2007).

bela atlantidea from mediterranean sea 3 Figs. 1A 9. Shells of Bela atlantidea (Knudsen, 1952): (1A 8) off Carini (38814 N13811 E), Palermo, Sicily, Italy, 75 m depth (12.1 5.1 mm). (9): off Marbella (36828 N4852 W), Spain, 30 40 m depth (10.5 4.3 mm).

4 paolo mariottini et al. Fig. 10 16. Paratype MNHN-21396 of Bela clarae Peňas & Rolán, 2008, Vallcarca, Sitges, Barcelona, Spain, 45 60 m depth (7.4 3.2 mm). DISCUSSION Differences between the genera Brachycythara and Bela are quite faint and mainly refer to the following: Brachycythara shells are smaller (4.0 8.6 mm), turreted, stouter, with the outer lip slightly thickened and with a sculpture of stout axial folds barely overridden in respect to the shells of the genus Bela (Powell, 1966: pp. 97, 117).

bela atlantidea from mediterranean sea 5 The turrid Brachycythara atlantidea was ascribed to the genus Brachycythara by Rolán & Otero-Schmitt (1999) with a short and general comment: The shells studied here have the typical characters of the genus, including the biconical profile. In our opinion this taxon better fits the genus Bela, since it shows: a dome-shaped multispiral protoconch consisting of three whorls (first smooth, second with axial riblets, third reticulated with spiral rows of tubercles); teleoconch of medium size for the genus, with an elongate fusiform shape, and with a spire about half of the total height; axial sculpture with 8 10 prominent, flexuous, and rounded axial and regularly spaced folds, with much broader interspaces; spiral sculpture of numerous very fine threads that densely alternate with bigger interspaces; subsutural thread shows well-marked axial denticles; aperture narrow, ovate, siphonal canal is short, narrow, and open; inner lip with a moderately developed parietal callus pad; outer lip thin or variced, according to the stage of growth, whether the lip coincides with an axial rib or an interspace; and shell colour uniformly yellowish-brown. Furthermore, the type species of Brachycythara (Cythara gibba Guppy, 1896) comes from the Miocene of the Caribbean area, while Recent species from the Caribbean, West Africa and the Mediterranean Sea are closer to those of the genus Bela. Therefore we are prone to consider Brachycythara as a fossil genus and to include Recent species in Bela. Taken together all these morphological features prompted us to move Brachycythara atlantidea to the genus Bela and ranking this turrid as Bela atlantidea (Knudsen, 1952) comb. nov. The recently described turrid Brachycythara beatriceae Mariottini, 2007 shows a strong morphological shell similarity with B. atlantidea, reflecting a close relationship, while it differs in some diagnostic characters such as: more ovate fusiform shell outline, bigger protoconch (700 750 mm); and the teleoconch colour which is invariantly white with a basal brown band. Interestingly, the distribution of B. beatriceae (Alboran Sea and West Sahara) represents a subset of that of B. atlantidea, suggesting that we are facing two sister species. The analyses carried out in this study that have driven the genus change of B. atlantidea, strongly suggest that B. beatriceae also be moved to the genus Bela. For this reason we changed the epithet to Bela beatriceae (Mariottini, 2007) comb. nov. After a morphological shell comparison between several specimens of B. atlantidea and the paratype MNHN-21396 of Bela clarae Peňas & Rolán, 2008 (see MATERIAL EXAMINED) we synonymized this taxon with B. atlantidea. Peňas et al. (2008) described as diagnostic characters of B. clarae a small protoconch and a different sculpture of the third protoconch whorl, though they recognized a strong similarity in shape and size of the teleoconch of B. clarae with B. atlantidea. However, the present comparative study clearly demonstrated that the protoconch is identical to the one of B. atlantidea in terms of size and sculpture. The small protoconch diameter reported for the holotype of B. clarae (476 mm) seems likely to be erroneous, as resulting from the re-measuring of the SEM picture published by Peňas et al. (2008: figure 27), showing a tilted protoconch. According to WoRMS (World Register of Marine Species, available at http://www.marinespecies.org/index.php) the Mediterranean (Alboran Sea) record of B. atlantidea is based on specimens brought in by fishing boats and requires confirmation. Albeit we report only one specimen of this turrid from Sicily, the freshness of the shell indicates that most probably this specimen was indeed living in the area sampled (Figure 17). Due to the synonymy between B. atlantidea and B. clarae, all the previous records of the latter one must be ascribed to B. atlantidea. From this new perspective, it results that the distribution of B. atlantidea is currently covering a wider range in the Mediterranean basin, including two Fig. 17. Mediterranean records of Bela atlantidea (Knudsen, 1952) and B. beatriceae Mariottini, 2007. B. atlantidea, circles; B. clarae, squares; B. beatriceae triangle.

6 paolo mariottini et al. other Italian spots (Gorgona Island, Tuscany Archipelago; off Pesaro, Adriatic Sea) and Malta as reported by Peňas et al. (2008) (Figure 17). Since the presence of B. atlantidea within the Mediterranean Sea is confirmed, this taxon can be added to the list of the Italian Mangeliidae. CONCLUSIONS This study focused nearly exclusively on shell characters of three mangeliine species that we considered related: (1) we included Brachycythara atlantidea (Knudsen, 1952) and Brachycythara beatriceae Mariottini, 2007 within the genus Bela sensu lato, so we proposed Bela atlantidea comb. nov. and Bela beatriceae comb. nov.; (2) we proposed the synonymy between B. atlantidea and Bela clarae Peňas & Rolán, 2008; and (3) the distribution of B. atlantidea in the Mediterranean basin was therefore updated including records of B. clarae. ACKNOWLEDGEMENTS The authors gratefully acknowledge Giuseppe Lucido (Palermo, Italy) who helped S.C. to collect molluscs by trawling with his fishing boat Annagaia. We are indebted to Ermanno Quaggiotto (Longare, Vicenza, Italy) and Giuseppe Bonomolo (Palermo, Italy) for their useful suggestions and to Ferdinando Meli (Capaci, Palermo, Italy) for cooperation and technical support. We express our gratitude to Virginie Heros (curator of the Mollusca section of MNHN) for the loan of the paratype of B. clarae and to two anonymous referees for their helpful comments that greatly improved the manuscript. REFERENCES Bouchet P., Kantor Yu. I., Sysoev A. and Puillandre N. (2011) A new operational classification of the Conoidea (Gastropoda). Journal of Molluscan Studies 77, 273 308. Bouchet P. and Taviani M. (1992) The Mediterranean deep-sea fauna: pseudopopulations of Atlantic species? Deep-Sea Research 39, 169 184. Guppy R.J.L. and Dall W.H. (1896) Description of the tertiary fossils from the Antillean region. Proceedings of the United States National Museum XIX, 303 331. Knudsen J. (1952) Marine prosobranchs of tropical West Africa collected by the Atlantide Expedition, 1945 46. Videnskabelige Meddelelser fra Dansk naturhistorisk Forening I Kjobenhavn 114, 129 185. Mariottini P. (2007) Brachycythara beatriceae, a new species from the Alboran Sea and the eastern Atlantic Ocean (Gastropoda: Neogastropoda: Conidae). Nautilus 121, 159 167. Peňas A., Rolán E. and Ballesteros M. (2008) Segunda adición a la fauna malacológica del litoral del Garraf (NE de la Península Ibérica). Iberus: Revista de la Sociedad Española de Malacología 26, 15 42. Powell A.W.B. (1966) The molluscan families Speightiidae and Turridae. Bulletin of the Auckland Institute and Museum 5, 1 157. Rolán E. and Otero-Schmitt J. (1999) The Family Turridae s. l. (Mollusca, Neogastropoda) in Angola, 2. Subfamily Mangeliinae Fischer, 1883. Argonauta XIII, 5 26. Smriglio C., Di Giulio A., Gubbioli F. and Mariottini P. (2007) Brachycythara atlantidea (Knudsen, 1952) (Gastropoda, Neogastropoda, Conidae), first report from the Western Mediterranean Sea. Basteria 71, 1 4. and Woodring W.P. (1928) Miocene molluscs from Bowden, Jamaica. Part 2: gastropods and discussion of results. Contributions to the geology and palaeontology of the West Indies. Carnegie Institute Washington Publication 385, 144 201. Correspondence should be addressed to: P. Mariottini Dipartimento di Biologia Università Roma Tre Viale Marconi 446, 00146 Rome, Italy email: mariotpa@uniroma3.it