A review of occurrence, distribution and alien status of Notodiaphana atlantica Ortea, Moro and Espinosa, 2013 and Liloa mongii (Audouin, 1826) (Mollusca: Heterobranchia) in the Mediterranean Sea

Both indexed and grey literature was reviewed for published Mediterranean records of Notodiaphana atlantica and Liloa mongii. The material examined in the present paper was collected from the bioclastic bottom by scuba diving or dredging. Comparisons were made with material illustrated in recent studies and samples collected from several localities, all listed below. The analyzed material is currently preserved in private collections (explanation under individual records).

Identifications follow the literature and/or type material referenced below. The updated taxonomy and nomenclature used in this study follow MolluscaBase (2020). Shells were examined using Kyowa SDZ-PL (Japan), Labolan S.L., Lomo MBC-10 (Russia), and Olympus SZ61 (Japan) stereomicroscopes, and measurements were carried out using an eyepiece micrometer. Selected shells and their details were also examined using Philips XL30 (the Netherlands) and Quanta200 (Massachusetts) scanning electron microscopes (SEMs) in the Centro de Apoyo Científico y Tecnológico a la Investigación (CACTI) – University of Vigo, after air drying and mounting on SEM stubs.

The following abbreviations and acronyms were used:

sh – empty shells;

Figure 1

Cylichnina multiquadrata (Oberling, 1970) – Cachia et al. (1993): 40 [Malta]; Sammut & Perrone (1998): 223 [Malta]; Cachia (1999): 105 [Malta]; Cachia et al. (2001): 125, 228–229, plate XX, Fig. 7 [Malta]; Cachia et al. (2004): 256 [Malta]; Cachia et al. (2019): 145 [Malta]

? Cylichnina multiquadrata (Oberling, 1970) – Buzzurro & Greppi (1997): 9 [Tasuçu, Turkey] — see Cecalupo et al. (2008); Micali (2014)

? Cylichna cf. mongii (Audouin, 1826) – Zenetos et al. (2004): 323 [Djerba Island, Tunisia and Akkum, Turkey, fide van Aartsen]

Cylichna cf mongii (Audouin, 1826) – Delongueville & Scaillet (2007): 56–58, Fig. 25 [Djerba, Tunisia; Side and Taşucu, Turkey]

Cylichnina multiquadrata (Oberling, 1970) – Cecalupo et al. (2008): 128–129, plate 75, Figs 4–8 [Djerba and Kerkennah Islands, Tunisia]

? Cylichnina cfr. mongii (Audouin, 1827) – Vazzana (2010): 71 [Scilla, Italy]; Vazzana (2011): 61 [Scilla, Italy] — see Micali (2014)

Cylichna cf. mongii sensu van Aartsen – Cossignani & Ardovini (2011): 371, figures [Malaga, Spain] — incorrectly reported from Spain, but found at Kerkennah Islands, Tunisia: see Cecalupo et al. (2008): plate 75, Figs 4–6 as Cylichnina multiquadrata and Micali (2014)

Cylichnina multiquadrata (Oberling, 1970) – Perna (2013): 243, figure [Scilla, Italy]

Notodiaphana atlantica Ortea, Moro et Espinosa, 2013 – Micali (2014): 499–504, Figs 3–6, 12–16 [Djerba, Tunisia; Messina, Augusta, and Linosa, Italy; Tétouan, Morocco] – Figs 13 and 15–16 incorrectly reported from Tunisia, but found in Cyprus: see Scaperrotta et al. (2016)

Retusa sp. – Oliver et al. (2015): 111, 142, 144, Figs 179–182 [Chafarinas Islands, Spain]

Notodiaphana atlantica Ortea, Moro & Espinosa, 2013 – Scaperrotta et al. (2016): 25, 110, figures [Kerkennah Islands, Tunisia and Protaras, Cyprus]

Notodiaphana atlantica Ortea, Moro et Espinosa, 2013 – Giacobbe & Renda (2018): 29, 30, 31, Fig. 6 [Capo d’Armi, Italy]

Notodiaphana atlantica Ortea, Moro & Espinosa, 2013 – Albano et al. (2020): 4065, Figs k–l [Rosh Carmel plateau and off Atlit, Israel]

Material examined: Morocco – 3 sh, Cabo Negro, 30 m, 2006 (CBC and APC). Italy – 1 sh, Isola delle Correnti (Portopalo di Capo Passero), 1.5 m, 28.viii.1992 (LTC); 6 sh, Pellaro, 26 m, vii.2009 (SBC, APC, and CBC); 1 lv, Cannitello, 40 m, vii.2009 (SBC). Tunisia – 3 sh, Djerba, 1 m, viii.1989 (CBC) [partially published in Micali (2014), namely Figs 3–5]; 17 sh, Sidi Youssef (Kerkennah), 0.5–1 m, vi.2009 (SBC) [partially published in Micali (2014), namely Figs 12 and 14 and Scaperrotta et al. (2016)]; Figures 1A–B. Greece – 2 sh, Malia, 4 m, 2015 (APC). Cyprus – 7 sh, Protaras, 26–30 m, vi.2011 (CBC and SBC) [partially published in Micali (2014), namely Figs 13, 15, and 16, incorrectly stated as coming from Djerba, Tunisia, and Scaperrotta et al. (2016)] (Figure 3A). Israel – 1 sh, Akko, 3 m, vi.1996 (LTC); 1 sh, Tel Aviv, 30 m, 14.×.2002 (CBC) (Figure 1C); 1 sh, Haifa, 18 m, unknown date (CBC).

Updated distribution: described from the Canary Islands (Ortea et al. 2013) [Lanzarote] and known from the western Atlantic {e.g. Redfern (2001): 154, plate 68 (Fig. 642A), plate 113 (Fig. 642B) as Cylichnid sp. A [Bahamas]; Valdés et al. (2006): 22–23 as Retusa sp. 1 [Venezuela]; Redfern (2013): 257 (Figs 722A–D) as Retusa sp. [Bahamas]; Ortea et al. (2013): 17, (Figs 4B, D) [Cuba]; Tunnell et al. (2010; 2014): 279 and 128, respectively, as Haminoea succinea (Conrad, 1846) [Texas, U.S.A.]; Zhang (2012): 171 (Fig. 671) as Atys mandrewii E.A. Smith, 1872 [Antigua and Barbuda]} and the eastern Atlantic {e.g. Mikkelsen (1995): 205 (Fig. 2E) as Retusa multiquadrata [Azores, Portugal]; Ávila et al. (1998): 502 as Retusa multiquadrata [Azores, Portugal]; Segers et al. (2009): 41, 251, 498–499 (plate 55, Figs 2–2a) as Retusa multiquadrata [Madeira, Portugal]; Ortea et al. (2013): 17, (Figs. 4C, 4E, plate 1) [Canaries, Spain]; Ortea & Moro (2018): 40 (Figs 1B–C) [Cabo Verde]; Delongueville et al. (2019): 40 (Fig. 4B) [Azores, Portugal]} and from the western to eastern part of the Mediterranean Sea (references and unpublished material listed above).

Shell description: small (up to 5 mm, usually much smaller), thin, translucent, almost twice as long as wide, subcylindrical-pyriform in outline, involute, with maximum width below the last whorl periphery. Aperture longer than spire, with anterior end rounded and wider than posterior end. Outer lip sharp, straight to slightly concave. Umbilicus narrow, partially covered by projection of thickened columellar lip. Columellar lip unfolded. Spire concave, deeply sunken, nearly covered by the last whorl, leaving a narrow apical umbilicus. Shell surface covered with thin, close, irregular spiral furrows. Spiral sculpture crossed, sometimes interrupted by orthocline, somewhat sinuous, axial growth lines, giving the surface a faintly reticulated appearance. Axial sculpture stronger within apical depression. Color uniformly whitish.

Remarks: supraspecific and specific taxonomy of N. atlantica has been widely debated in the recent literature. In fact, its generic assignment has been recently questioned by Oskars et al. (2015), who suggested that the genus Notodiaphana Thiele, 1917 and the family Notodiaphanidae Thiele, 1931 should be considered as nomina dubia. However, we hereby used it cautiously according to MolluscaBase (2020). Moreover, Giacobbe & Renda (2018) suggested that N. atlantica may comprise a complex of species based on a putative disjunct distribution in the western Atlantic and the Mediterranean Sea. Based on the present results, however, N. atlantica shows a broad amphi-Atlantic distribution, ranging uninterruptedly from the western Atlantic Ocean to the eastern Mediterranean Sea, having also been widely recorded from Macaronesia (eastern Atlantic) as Retusa multiquadrata (see Updated distribution). Nonetheless, an integrative taxonomic approach could confirm or refute this statement. With regard to its distribution in the Mediterranean Sea, Micali (2014) originally reported N. atlantica from the western and central parts of the basin, although according to subsequent reports by Scaperrotta et al. (2016) and Albano et al. (2020), its distribution also includes the eastern Mediterranean. The species has been mostly reported from the basin as Cylichnina multiquadrata (Oberling, 1970), a taxon whose identity is still uncertain (Crocetta & Tringali 2015; Crocetta et al. 2015), and Cylichnina/Cylichna (cf) mongii (Audouin, 1826), which is discussed below. Although most of the records listed above illustrated the material examined, thus confirming what is reported here, three records (Buzzurro & Greppi 1997; Zenetos et al. 2004; Vazzana 2010) lack images and are listed here with a preceding question mark. However, as N. atlantica is widespread at the localities investigated there, the three questionable records presumably also referred to N. atlantica. The updated distribution of N. atlantica in the Mediterranean Sea is reported in Figure 2.

Figure 2

Not Cylichnina cfr. mongii (Audouin, 1827) – Cecalupo & Quadri (1996): 98–99 (plate 3, Figs 1–1a–1b) [Kyrenia, Cyprus] – figures first re-published online (Coppini 2002) and then in print (Coppini 2004); see Ortea et al. (2013)

Not Cylichna cf. mongii (Audouin, 1826) – Zenetos et al. (2004): 323 [Island of Djerba, Tunisia and Akkum, Turkey, fide van Aartsen]

Not Cylichnina cfr. mongii – Repetto et al. (2005): 258 (Fig. 1136) [Eastern Mediterranean Sea]

Not Cylichna cf mongii (Audouin, 1826) – Delongueville & Scaillet (2007): 56–58, Fig. 25 [Djerba, Tunisia; Side and Taşucu, Turkey]

Not Cylichnina cfr. mongii (Audouin, 1827) – Vazzana (2010): 71 [Scilla, Italy]; Vazzana (2011): 61 [Scilla, Italy] – see Micali (2014)

Not Cylichna cf. mongii sensu van Aartsen – Cossignani & Ardovini (2011): 371, figures [Malaga, Spain] – incorrectly reported from Spain, but found at the Kerkennah Islands, Tunisia: see Cecalupo et al. (2008): plate 75, Figs 4–6 as Cylichnina multiquadrata and Micali (2014)

Not Cylichnina mongii (Audouin, 1827) – Perna (2013): 243, figure [Kos, Greece]

Shell description (based on the holotype): minute (1.5 mm) but not thin, opaque, almost twice as long as wide, ovate-cylindrical in outline, involuted, with maximum width around the middle of the last whorl periphery. Aperture longer than spire, with anterior end rounded and wider than posterior end. Outer lip apparently broken, regularly curved. Umbilicus narrow, partially covered by projection of thickened columellar lip. Columellar lip unfolded. Spire concave, deeply sunken. Shell surface covered with thin, close, irregular spiral furrows. Spiral sculpture crossed by orthocline axial growth lines, giving the surface a reticulated appearance. Axial sculpture present within apical depression. Color whitish.

Remarks: Liloa mongii was originally described from an unknown locality in Egypt, very likely from the Egyptian Red Sea; see Amati et al. (2019) for discussion. The holotype of L. mongii, most likely a juvenile (~1.5 mm high), was described by Bouchet & Danrigal (1982: Fig. 58) and Valdés & Héros (1998: Fig. 4A), whereas Ortea et al. (2013: Fig. 6) erroneously assigned the holotypes of both Bulla girardi Audouin, 1826 (namely Fig. 6A) and Bulla mongii Audouin, 1826 (namely Fig. 6B) to the latter species. Based on the recent literature, L. mongii appears to have a wide distribution covering a large part of the Indo-Pacific region and the Red Sea, where it was mostly recorded under its junior synonym Bulla curta A. Adams, 1850 (e.g. Micali 2014; Too et al. 2014; Oskars et al. 2019). Moreover, Micali (2014) reported it also from the Bitter Lakes and the Mediterranean Sea, where it was considered a Lessepsian immigrant. However, the synonymy between L. mongii and L. curta is poorly supported, the variability and growth of “true” L. mongii was never properly investigated, and a review of the recent literature concerning the Indo-Pacific region showed that L. curta shows high variability in shell shape and sculpture and may comprise a complex of species. Finally, the congeneric Liloa porcellana (Gould, 1859) may fall within the range of variability of the two Liloa species mentioned above, or all these species may have been frequently mixed up in the recent literature (e.g. Higo et al. 2001; Poppe 2008; Rushmore-Villaume 2008; Severns 2011; Micali 2014; Chaban 2016; Okutani 2017). With regard to the records published from the Mediterranean Sea, the majority of them concern N. atlantica (see above). On the other hand, the record from Cyprus described by Cecalupo & Quadri (1996) and considered by Micali (2014) as the only confirmed record of L. mongii from the Mediterranean Sea, is based on three empty shells whose sizes cannot be fully determined. Two of them (Figs 1, 1a) show an irregular outline, with the largest one (Fig. 1) showing a spiral striate or even reticulate sculpture, whereas the sculpture is not well visible in the smallest specimen (Fig. 1a). The third shell (Fig. 1b) shows an outline resembling N. atlantica, but the figure is completely blurred. Noteworthy, the largest of these specimens was also presumably redrawn in the malacological atlas by Repetto et al. (2005). Based on the photos published by Cecalupo & Quadri (1996), these three specimens do not correspond with certainty to N. atlantica, and not even to the holotype of L. mongii or L. mongii sensu Micali (2014). Unfortunately, the specimens figured by Cecalupo & Quadri (1996) cannot be re-examined due to the untimely death of the latter author in 1998 (A. Cecalupo, personal communication), so they remain here as unidentified. Finally, the record by Perna (2013) from Kos (Greece) is based on a shell with a total height of 1.5 mm, thus comparable to the holotype of L. mongii. However, it is completely different in shape and sculpture from L. mongii. A comparative table illustrating N. atlantica, the holotype of L. mongii, L. mongii sensu Perna (2013) and L. mongii sensu Micali (2014) is provided in Figure 3.

Figure 3