Aplysia punctata, (CUVIER, 1803)

Golestani, Haleh, Crocetta, Fabio, Padula, Vinicius, Camacho-García, Yolanda, Langeneck, Joachim, Poursanidis, Dimitris, Pola, Marta, Yokeş, M. Baki, Cervera, Juan Lucas, Jung, Dae-Wui, Gosliner, Terrence M., Araya, Juan Francisco, Hooker, Yuri, Schrödl, Michael & Valdés, Ángel, 2019, The little Aplysia coming of age: from one species to a complex of species complexes in Aplysia parvula (Mollusca: Gastropoda: Heterobranchia), Zoological Journal of the Linnean Society 187, pp. 279-330 : 317-319

APLYSIA PUNCTATA ( CUVIER, 1803)

( FIGS 22–25)

Aplysia rosea Rathke, 1799: 147 , pl. 3, fig. 12A–B [suppressed by ICZN (1955: Opinion 355)]. Type locality: Not stated. Type: Not known.

Laplysia punctata Cuvier, 1803: 310 , pl. 1, fig. 2. Type locality: Not stated. Type: Probably lost, not found at MNHN ( Valdés & Héros, 1998).

Aplysia hybrida J. Sowerby, 1806: 111–113 , pl. 53. Type locality: St. Michael’s Mount , Cornwall, England, UK. Type: Probably lost, not found at NHMUK (A. Salvador, pers. comm.).

? Aplysia mustelina Pennant, 1812 (ex. Davies): 79, pl. 22. Type locality: Tenby, Pembrokeshire, Wales, UK. Type: Probably lost, not found at NHMUK (A. Salvador, pers. comm.).

Aplysia nigromarginata Risso, 1818: 375 . Type locality: Nice, France. Type: Probably lost ( Arnaud, 1977), not found at MNHN ( Valdés & Héros, 1998) or at MHNG (E. Tardy, pers. comm.).

Aplysia stellata Risso, 1818: 375 . Type locality: Nice, France. Type: Probably lost ( Arnaud, 1977), not found at MNHN ( Valdés & Héros, 1998) or at MHNG (E. Tardy, pers. comm.).

Aplysia unicolor Risso, 1818: 374–375 . Type locality: Nice, France. Type: Probably lost ( Arnaud, 1977), not found at MNHN ( Valdés & Héros, 1998) or at MHNG (E. Tardy, pers. comm.).

Aplysia marginata de Blainville, 1823: 326 . Type locality: Unknown. Type: Location unknown, not found at MNHN ( Valdés & Héros, 1998).

Aplysia cuvieri Delle Chiaje, 1823 –1824 (1823): 41, 71. Type locality: Naples, Italy. Type: Location unknown.

Aplysia virescente Risso, 1826: 42–43 . Type locality: Nice, France. Type: Probably lost ( Arnaud, 1977), not found at MNHN ( Valdés & Héros, 1998) or at MHNG (E. Tardy, pers. comm.).

Aplysia ferussaci Rang, 1828: 66 , pl. 19, figs 6–9. Type locality: Unknown. Type: Probably lost, not found at MNHN ( Valdés & Héros, 1998).

Aplysia longicornis Rang, 1828: 66 , pl. 19, figs 1–4. Type locality: French Mediterranean coast, France. Type: Probably lost, not found at MNHN ( Valdés & Héros, 1998).

Aplysia dumortieri Cantraine, 1835: 386 . Type locality: ‘Raguza Vechia’ (= Cavtat), Croatia. Type: Unknown

Aplysia guttata M. Sars, 1840: 213–216 , pl. 6, figs ( Aplysia )A–G. Type locality: Not stated. Type: Unknown

Aplysia nexa W. Thompson, 1845: 313–314 , pl. 19, fig. 8. Type locality: Torbay, England and Belfast Bay, Northern Ireland, UK. Type: Probably lost, not found at NHMUK (A. Salvador, pers. comm.).

Aplysia varians Leach, 1847: 268 (nomen nudum); Leach, 1852: 33. Type locality: Cornwall, Devon and Dorset, England, UK. Type: Probably lost, not found at NHMUK (A. Salvador, pers. comm.).

? Esmia griffithsiana Leach, 1852: 34 , pl. 7, figs 8–10. Type locality: Torbay, England, UK. Type: Probably lost, not found at NHMUK (A. Salvador, pers. comm.).

Aplysia albopunctata Deshayes, 1839 –53 (1853): 59, pl. 92, figs 1–2. Type locality: Not stated. Type: Probably lost, not found at MNHN ( Valdés & Héros, 1998).

Additional material examined: Santander, Spain, May 2013, three specimens 8–22 mm preserved length ( CPIC 01424 , isolate HG78). Bahía de Cádiz, Spain, 3 March 2006, one specimen 19 mm preserved length ( CPIC 1359 , isolate HG24). Cap l’Abeille, Banyuls sur Mer , France, 8-m depth, 22 May 2014, one specimen 13 mm preserved length ( CPIC 01361 , isolate HG51). Gallipoli, Italy, 3 April 2009, one specimen 12 mm preserved length ( CPIC 01355 , isolate HG14); 3 April 2009, one specimen 19 mm preserved length ( CPIC 01358 , isolate HG26). Livorno, Italy, 19 April 2014, two specimens 12–16 mm preserved length ( CPIC 01379 , isolate HG48). Kato Zakros, Crete, Greece, 9 April 2009, five specimens 6–15 mm preserved length ( CPIC 02181 , isolate HG33); two specimens 11–14 mm preserved length ( CPIC 01387 , isolate HG87). Agia Pelagia , Crete, Greece, one specimen 18 mm preserved length ( CPIC 01388 , isolate HG86) .

Description

External anatomy: Animal oval to elongate, wider in visceral region, narrowing gradually towards head and more abruptly towards tail; visceral hump proportionally very large, elongate, well-differentiated from the rest of the body, occupying about than 1/2 of body length; mantle foramen very large, oval, on posterior left side of visceral hump, not elevated; parapodia broad, fused posteriorly, sometimes joined anteriorly, forming several folds; rhinophores and oral tentacles relatively short, enrolled, with a small basal projections in each oral tentacle; siphon wide, relatively short, protruding slightly above parapodia. Colour pale orange to reddish-brown, with scattered large white spots, some specimens with numerous additional small white dots, others lacking white, covered with brown dots; parapodia edged in white, sometimes with a broad submarginal black or brown band, often with white dots; rhinophores and oral tentacles same colour as body, some animals with black or brown tips and white dots; mantle foramen with thin white inner edge.

Internal anatomy: Shell oval, widest near mid-length; posterior end regularly curved, right slightly concave adjacent to protoconch; rachidian tooth with robust, triangular central cusp bearing multiple sharp denticles, 2–3 lateral cusps on each side of central cusp, typically lacking denticles; lateral teeth with central cusp denticulated on both sides, larger tooth or secondary cusps near each side of base; up to five simple outer teeth. Radular formula 30 × 4.10.1.10. 4 in an 18 mm preserved length specimen from Greece ( CPIC 01388, isolate HG86). Jaw with cylindrical, elongated elements with 1–2 cusps at tips. Penis very elongate, narrow, with a single retractor muscles, and simple tip, lacking papillae.

Range: North-eastern Atlantic Ocean from Norway and the Baltic Sea to Macaronesia ( Eales, 1960; Ávila et al., 1998, 2000; Wirtz, 1999) and throughout the Mediterranean ( Eales, 1960).

Remarks

The name Aplysia punctata has been used for a widespread species occurring in the north-eastern Atlantic (including Greenland) from Norway to the Canary Islands, the Mediterranean and the Baltic Sea ( Eales, 1960), with more recent records from the Azores ( Ávila et al., 1998, 2000) and Madeira ( Wirtz, 1999). Pilsbry (1895 –96), Engel (1936) and Eales (1960) compiled a list of synonyms (listed above) and provided a comprehensive description of this species.

In this study we sequenced a number of specimens collected in the Mediterranean and the Atlantic coast of Europe (including the Azores) identified as A. parvula . However, the mtDNA sequences of these specimens are similar to sequences obtained from GenBank of specimens identified as A. punctata and collected from the eastern Atlantic, as far north as Germany, but different from other specimens of the A. parvula species complexes from other regions. The only mtDNA sequences that displayed consistent differences were obtained from samples collected in the Azores that display 17 substitutions in COI versus animals from the European mainland. Thus, based on the analyses of mtDNA sequences, we cannot confirm the presence of any species of the A. parvula species complexes in the eastern Atlantic or Mediterranean with the exception of A. punctata . These results are surprising, considering the specimens sequenced from these areas were phenotypically similar to A. parvula s.l. Furthermore, the examination of the penial morphology of our specimens confirmed the presence of a single retractor muscle, also consistent with the characteristics of A. punctata . Finally, sequence data from the nDNA gene histone H3 confirmed that most of the specimens from the Mediterranean and the Atlantic coast of Europe (including the Azores) were genetically different from other species of the A. parvula species complexes from other areas in the Atlantic Ocean and beyond. However, a specimen collected in the Azores (HG20) and a specimen collected in Italy (HG19) are heterozygotes, with one allele from A. punctata and another from A. ghanimii . The genetic makeup of these two individuals suggests they could constitute hybrids between these two species, although it could also be the result of incomplete lineage sorting. If hybridization is confirmed, it potentially suggests limited genetic introgression of A. ghanimii into the Mediterranean and eastern Atlantic populations of A. punctata .

These results contradict the previous hypothesis ( Eales, 1970; Bebbington, 1975; Bebbington & Brown, 1975) that the Mediterranean has been broadly invaded by A. parvula . If any invasion has occurred, it was a limited introgression of A. ghanimii nDNA into native A. punctata populations. Phenotypically, some Mediterranean specimens of A. punctata appear to match the external characteristics of other members of the A. parvula species complexes, but a closer examination suggests otherwise. For example, the body of the Mediterranean and Eastern Atlantic animals identified as A. parvula have shorter bodies with more triangular tails than in any other species of A. parvula s.l. It appears that the only trait linking Mediterranean and eastern Atlantic specimens with other species of the A. parvula species complexes is the external coloration. It is widely agreed that the suggested invasion of A. parvula of the Mediterranean started with Swennen’s (1961) report of specimens with a distinctive black band on the edge of the parapodia collected in Turkey. However, the penial morphology of those specimens was consistent with that of A. punctata (see Bebbington, 1977), highlighting the difficulties to properly identify these two species using morphology alone. Moreover, a review of the literature reveals that Swennen’s (1961) report was not the first Mediterranean record of A. parvula -like specimens. Risso (1818) described Aplysia nigromarginata from Nice, France, as being black in colour with a dark black rim of the mantle and dark tentacles. This description matches the colour typically described for A. parvula , including Mediterranean animals, but Eales (1960) regarded A. nigromarginata it as a synonym of A. punctata .

As mentioned above, the only specimens from the Mediterranean and the eastern Atlantic that display genetic differences are those from the Azores, which form a well-supported clade ( Fig. 2A) and are recovered as a distinct species in the ABGD analysis ( Table 2). Although this population probably constitutes a distinct species, it is not described herein due to a lack of complete specimens; only tissue samples were obtained.