Atys jeffreysi ( Weinkauff, 1866 )

Oskars, Trond Roger, Mifsud, Constantine & Malaquias, Manuel António E., 2017, Redescription of the Cephalaspidea gastropod Atys jeffreysi (Weinkauff, 1866) (Haminoeidae), with a discussion on the phylogenetic affinities of the Mediterranean species of the genus, Journal of Natural History 51 (27 - 28), pp. 1593-1608 : 1597-1601

Atys jeffreysi ( Weinkauff, 1866)

( Figures 1 (a), 2, 3)

Bulla ovulata Brocchi, 1814 sensu Jeffreys, 1856, p. 188 , pl. 2, figures 18, 19; Weinkauff

1862, p. 337. Bulla (Cylichna) jeffreysi Weinkauff, 1866, p. 238 . Haminea ovulata Brocchi : Brusina 1866, p. 83 (specimens seen by Weinkauff (1868, p. 199)). Cylichna jeffreysi: Weinkauff 1868, p. 199 . Roxaniella jeffreysi: Monterosato 1884, p. 145 . Atys (Roxaniella) jeffreysi: Nordsieck 1972, p. 30 , 31, pl. 4, figure 23. Atys jeffreysi: Pilsbry 1895, p. 277 , pl. 59, figures 1 and 2; Thompson et al. 1985, p. 84, 89,

figure 7A, pl. 9D (correct caption pl. 10D); Malaquias et al. 2002, p. 76; Trono 2006, p.

80, 81, figure 3(d). Cachia and Mifsud 2007, p. 45, figures 2 and 5; Templado et al. 2011,

p. 421; Crocetta et al. 2015, p. 58 (tab. 2).

Type locality

La Spezia, Italy, ‘Piedemonte Coast’ (Ligurian Sea), Mediterranean Sea, ( Jeffreys 1856, p. 188; Weinkauff 1866, p. 238).

Material examined

Mediterranean Sea, La Spezia, Italy: Locality mentioned in text ( Jeffreys 1856, p. 188), NHMUK labels marked only with ‘Piedemonte Coast’ . Fragments of 2 shells (syntypes), 1 complete shell, NHMUK 196472 (syntype), H = 5.1 mm . Mediterranean Sea, Gnejna Bay , Malta, 1 spc. (dissected) , ZMBN 81802 , H = 3 mm . Mediterranean Sea , Gnejna Bay, Malta, several empty shells, ZMBN 81800 , H = 2–5 mm . Mediterranean Sea, Gnejna Bay , Malta, 1 spc. (whole specimen sequenced) , ZMBN 81800 , H = 2 mm .

External anatomy ( Figure 1 (a))

Animal translucent covered with white dots; mantle under shell covered with red to rusty brown blotches; scattered red blotches also present on cephalic shield and parapodial lobes. Cephalic shield, short, broad, rounded, bilobed; small cephalic lobes present, eyes visible. Parapodial lobes, triangular.

Shell ( Figures 2 (a–c), 3(a) and 3(b))

Shell whitish transparent to yellowish transparent, cylindrical, truncated at both ends. Spiral striae covers entire shell; made of fused, rounded indentations; alternating thick and thin striae. Axial striae (growth lines) cross spiral striae generating a decussate pattern. Aperture runs the length of the shell, narrowing apically; upper lip extends beyond apex, arching to upper columella; not folded neither twisted at apex. Columellar lip with slight fold, small umbilical groove behind columellar fold present.

Radula

Radula formula 20 × 4.1.4. All teeth lacking denticulation ( Thompson et al. 1985).

Gizzard plates ( Figure 2 (c–d))

Three gizzard plates with 12–13 ridges each. Top edge of ridges covered by single rows of tiny rods with pointed tips; front and back sides of ridges smooth. Pseudo-rachis between ridges present.

Reproductive system ( Figure 2 (e))

Male reproductive system elongate and cylindrical with three distinct parts; penial sheath, elongate seminal duct narrowing distally, pear-shaped prostate, narrowing proximally. Several prostatic glands visible inside prostate. Elongate penial papilla.

Distribution

Widely distributed in the Mediterranean Sea from the Levantine coast in the east to the Sea of Alborán in the west. Turkey: Sea of Marmara, Aegean Sea and Levantine Sea ( Öztürk et al. 2014). Croatia: Zadar (as Zara), Dalmatian Coast, Adriatic Sea ( Brusina 1866; Weinkauff 1868). Greece: Patras Bay, Cretan Archipelago, Ionian Sea ( Thompson et al. 1985; Crocetta et al. 2015). Italy: Salento, Tyrrhenian Sea and La Spezia (type locality), Ligurian Sea ( Jeffreys 1856; Weinkauff 1866; Trono 2006), Malta: Gnejna Bay, Salina Bay, Fomm ir-Rih Bay ( Cachia and Mifsud 2007; present study). Algeria: Sidi Fredj (as Sidi- Ferruch), Staoueli ( Weinkauff 1862). Spain: Alborán Is., Catalonia and Andalusía coastlines ( Peñas et al. 2006; Ballesteros 2007; Templado et al. 2011). Madeira and the Canary Is.: ( Malaquias et al. 2002; Moro et al. 2003; Cervera et al. 2004).

Remarks

Jeffreys (1856) studied a shell from the MacAndrew collection housed at the NHMUK identified as Cylichna strigella Lovén, 1846 that Jeffreys re-identified as Bulla ovulata Brocchi, 1814 . Jeffreys (1856) did not specify which shell this one was and where it was collected, and despite our efforts we could not trace it. Nevertheless, the only image known to Jeffreys of B. ovulata was that figured in Brocchi (1814, p. 277, 635, pl. 1, figure 8), which was in the words of Jeffreys (1856, p. 188): ‘... not, to my mind, satisfactory’, and for this reason Jeffreys included on his study about the molluscs of the Piedmontese coast (Ligurian Sea) two drawings of one of his specimens collected at La Spezia, Italy ( Jeffreys 1856, p. 188, pl. 2, figures 18, 19; NHMUK 196472; Figure 2 ).

Weinkauff (1866, p. 238) considered B. ovulata a junior synonym of the fossil species Atys brocchii ( Michelotti, 1847) (as Bulla (Cylichna) brocchii ) and the Mediterranean shells of ‘ Bulla ovulata ’ identified by Jeffreys (1856) a new species, which he named Bulla (Cylichna) jeffreysi ( Weinkauff, 1866) . The syntypes of this latter species include one complete shell and several additional shell fragments ( Figure 2 (c)), which together seem to make three shells. Jeffreys (1856) and Weinkauff (1866) did not mention the number of shells they studied, but the labels following the syntypes also refer to three shells ( Figure 2 (c)). Moreover, a letter by Clay Carlson dated 4 February 1993 and addressed to Dr David Reid (former Merit Researcher of Mollusca at the NHMUK) which is deposited together with the syntypes’ lot also refers to the existence of three shells [ Carlson and Hoff (2000) have only briefly commented on this material in a comparison to the Pacific species Atys multistriatus ].

Weinkauff (1868, p. 199) included a description of A. jeffreysi to complement the drawings of Jeffreys (1856) to differentiate it from Atys brocchii and mentioned a shell of 8 mm height. The only complete syntype measures 5.1 mm and there are subtle differences between this syntype and Weinkauff’ s (1868) description (more pronounced striae in the middle of the shell) and also between the shape of the columellar lip compared to the drawing included in Jeffreys (1856) ( Figure 2 (a), 2(b)). It remains speculative, but most likely these differences stem from the fact that both Jeffreys (1856) and Weinkauff (1868) described a different shell from the only one remaining in the original syntype lot (NHMUK 196472, Figure 2 (c)).

Phylogenetic analysis

Our COI phylogenetic tree includes all available DNA sequences for species of the genera Atys , Liloa and Aliculastrum , encompassing about 30% of the worldwide diversity of Atys species (see Discussion). The tree was poorly resolved and no genera were recovered monophyletic, but this is expected as the analysis was based on a single gene ( Oskars et al. 2015). Atys jeffreysi and A. macandrewii were not rendered sister lineages; A. macandrewii was sister to the Central Pacific species A. ukulele with maximum support ( Figure 4 , PP = 1), whereas A. jeffreysi was nested within a clade of Indo-West Pacific species that received moderate support ( Figure 4 , PP = 0.92) in a sister position to the West Pacific species A. pittmani , nevertheless without support ( Figure 4 , PP = 0.53).

Genetic distance analysis (uncorrected p -distance; Table 2) rendered a difference of 21.6% between A. macandrewii and A. jeffreysi . This is close to the maximum distance found among all Atys species analysed (21.8% between A. ukulele and A. pittmani ). The minimum distance found was 8.7% between the Central Pacific A. ukulele and the Atlantic/Mediterranean A. macandrewii . The sister pair A. naucum and A. kuhnsi differed 11.9%, whereas the two specimens of A. semistriatus differed 11.3%, most likely indicating cryptic speciation in this widespread species.

Figures

Figure 1. (a). Atys jeffreysi, dorsal view live animal, H = 6 mm, Fomm ir-Rih Bay, Malta, 30–40 m, 2006. (b). Atys macandrewii, dorsal view live animal, H = 5 mm, Gnejna Bay, 40 m, 1996. Photographs courtesy of C. Mifsud.

Figure 2. Atys jeffreysi. (a) Apertural view (left image) and adpertural view (right image) of syntype of Bulla (Cylichna) jeffreysi (NHMUK 196472, H = 5.1 mm). (b) Illustration of one of the syntypes taken from Jeffreys (1856: pl. 2, figures 18, 19); apertural view (left image) and adpertural view (right image). (c) Complete shell and shell fragments of syntypes (NHMUK 196472) and accompanying labels (the authorship of B. ovulata is wrongly attributed to Lamarck 1804 in the label). Scale bar = 5 mm.

Figure 4. Bayesian phylogenetic tree based on partial sequences of the COI gene. Figures on nodes are posterior probabilities, scale bar show branch lengths. Species names followed by geographical range (Indo-Pacific distributions taken from Too et al. 2014; Gosliner et al. 2015).