Runcina aurata, GARCIA ET AL., 1986

Araujo, Ana Karla, Pola, Marta, Malaquias, Manuel Antonio E, Ballesteros, Manuel, Vitale, Fabio & Cervera, Juan Lucas, 2022, Molecular phylogeny of European Runcinida (Gastropoda, Heterobranchia): the discover of an unexpected pool of complex species, with special reference to the case of Runcina coronata, Zoological Journal of the Linnean Society 194 (3), pp. 761-788 : 773-779

RUNCINA AURATA GARCÍA ET AL., 1986

( FIGS 3C–F , 4D–F , 5B , 6B )

Type locality: Club La Hacienda , Cádiz, Spain (36º14’18”N; 5º18’36”W)

Examined material: MNCN 15.05 /91500, La Caleta (Cádiz) (36º31’59”N; 6º18’31”W), Andalusia, southwestern Spain, 8 April 2019, 3.5 mm living animal, depth 0.5–1.0 m (dissected and sequenced) . MNCN 15.05 /88106, La Caleta (Cádiz) (36º31’59”N; 6º18’31”W), Andalusia, south-western Spain, coll. Josep Romà, 18 April 2015, 2 mm in length preserved, depth 0.5–1.0 m. (dissected and sequenced) . MNCN 15.05 /88107, La Caleta (Cádiz) (36º31’59”N; 6º18’31”W), Andalusia south-western, Spain, coll. Josep Romà, 18 April 2015, 2 mm in length preserved, depth 0.5–1.0 m (dissected and sequenced) . MNCN: ADN 118948 , La Caleta (Cádiz) (36º31’59”N; 6º18’31”W), Andalusia southwestern, Spain, coll. Josep Romà, 17 May 2015, 1.5 mm in length preserved, depth 0.5–1.0 m (dissected and sequenced) . MNCN: ADN 118950 , El Chato (Cádiz) (36º28’39”N; 6º15’49”W), Andalusia south-western, Spain, coll. Ana Bartual, 13 April 2015, 1 mm in length preserved, depth 0.5–1.0 m (dissected and sequenced) .

External morphology ( Fig. 3C–F ): Living specimen 3.5 mm length and preserved specimens 1–2 mm length. Body elongated and moderately broad. Lateral grooves on both sides between notum and foot. Anterior part of notum (‘head’) slightly bilobed. Posterior part of notum rounded. Propodium rounded, metapodium pointed. Foot as wide as notum. Foot extended beyond notum on rear part. Ground colour of body translucent pale fawn or yellowish. Digestive system visible as a broad brownish blotch. White spots on central zone of notum, behind eyes forming triangular patches and anterior to notum end. White spots maybe also absent. Black dots dispersed on notum and more concentrated on head zone. Eyes inconspicuous. Dark band on middle of dorsal surface of foot. Black dots may be present on ventral surface of foot. Four rounded and relatively large gills laminae to the right of anus. Gills yellowish with slightly brown margins. Anus located in median line of body, beneath the end of notum.

Internal anatomy ( Figs 4D–F , 5B , 6B ): Radular formulae 12 × 1.1.1 (MNCN 15.05/88106) and 13 × 1.1.1 (MNCN 15.05/91500). Rachidian tooth bilobed with long and smooth lateral wings on each side. Central part contains pair of pads, each possessing 10–11 long, slender, pointed denticles. Size of denticles variable. Small denticles between large denticles. Small depression present between pads, with minute denticle present ( Fig. 4D ). Lateral teeth denticulate, elongate, hooked shape with 35–36 long, pointed and samesize denticles ( Fig. 4E ). Triangular jaws present. Four gizzard plates with seven to nine crests ( Fig. 4F ). Shell absent. Reproductive system monaulic. Female gland mass placed on right side and behind digestive gland, opening to exterior through small size common genital duct ( Fig. 5B ). Male pore opens next to mouth, on the right side. Elongated and cylindrical male copulatory organ. Penial papilla not observed. Cylindrical and long prostate gland ends in slender and small seminal vesicle with black pigmentation ( Fig. 6B ).

Distribution: Cádiz, Strait of Gibraltar, Malaga and Murcia (southern Spain) ( Templado, 1984; Garcia et al., 1986) and Azores Islands ( Portugal) ( Gosliner, 1990).

Remarks: Runcina coronata has been considered a taxonomically difficult species (see Introduction). Originally described from Brehat (Atlantic coast of France), this species was first reported in the Mediterranean Sea by Vayssière (1883) who identified specimens from Marseille (Mediterranean coast of France) as R. coronata . However, Burn (1963), based on morphological differences, especially the shape of the body and the colour pattern, suggested the specimens identified by Vayssière (1883) could be R. calaritana . We cannot confidently attribute those specimens to a specific species, but we agree with Burn (1963) that they probably do not correspond to R. coronata . Pruvot-Fol (1954), and Cervera et al. (1991) regarded R. calaritana (Gulf of Cagliari, Sardinia, Italy) and R. aurata (from around the Strait of Gibraltar) conspecific with R. coronata . This problematic has ultimately created the perception that R. coronata was present in the Mediterranean Sea ( Schmekel & Cappellato, 2002; Cervera et al., 2004; Ballesteros et al., 2016).

In general, the external and internal morphology of our specimens of R. coronata from Swanage ( England) are consistent with the original description of the species ( Quatrefages, 1844), and with the description provided by Schmekel & Cappellato (2002) based on specimens from Roscoff (Atlantic coast of France) and Plymouth (south of England). However, compared with the description provided by García et al. (1986; specimens from the Strait of Gibraltar), our animals from England exhibit several differences, mainly in the shape of the body and colour pattern. The anterior and posterior ends of the notum are rounded, while in Spanish specimens it is pointed ( García et al., 1986). The colour pattern of our specimens ( Fig. 3A, B ) differs drastically from those from the Strait of Gibraltar, which have a uniformly dark colour pattern, two whitish bands on both sides of the head and one white small band on the posterior right side of the notum ( García et al., 1986). This suggests that likely specimens attributed to R. coronata by García et al. (1986) belong to a distinct species.

The original description of R. coronata describes briefly the male copulatory organ as ‘a rather short testicular bag in the shape of a “club”, with a seminal vesicle sometimes absent ( Quatrefages, 1844).’ Kress (1977) studied specimens from Plymouth ( England) and provided additional anatomical data on the reproductive system. Comparatively, our specimens from Swanage ( England) exhibit a similarly long and cylindrical prostate, but a slightly different seminal vesicle and common genital duct. Kress (1977) referred to a seminal vesicle ‘considerably shorter than prostate’ and a common genital duct forming a long loop, whereas in our material the seminal vesicle was approximately half the size of the prostate and the common genital duct was short ( Fig. 6A ).

The species R. aurata was described by García et al. (1986) from the southern coast of Spain (Cádiz, Strait of Gibraltar and Malaga). Gosliner (1990) reported the species from the Azores and suggested that a specimen illustrated and depicted by Thompson & Brodie (1988: fig. 1E) from Plymouth as R. coronata was most likely R. aurata . Despite the fact that the description and illustration provided by Thompson & Brodie (1988) are vague and lacking important information, the reference to the presence of a light area surrounding the eyes, suggests their identification as R. coronata to be correct.

The features of our specimens collected in Cádiz ( Spain) are consistent with the original description of the species R. aurata ( García et al., 1986) . Externally, they differ from R. coronata by having a translucent yellow colour with black spots on the notum and on the ventral surface of the foot ( Fig. 3 ; Table 4). Also, the number of gills is distinct: three gills in R. coronate , while our animals of R. aurata from Cádiz have four gills ( Table 4). The original description of R. aurata refers, in fact, to three gills only, but the authors did not seem to have thoroughly looked at this character, which is difficult if not examined properly and across several specimens ( García et al., 1986).

Concerning the radula, we observed some subtle differences between R. aurata and R. coronata , namely in the number of radular rows and shape of the denticles in the pads of the rachidian teeth ( Table 4). However, in runcinids, these features can vary, even within species ( Schmekel & Cappellato, 2001; 2002; Araujo et al. 2019), and are, therefore, difficult to use in species identification. Regarding the gizzard plates, our specimens of R. coronata show ten crests in each plate, while in our animals of R. aurata it ranges from seven to nine, which is consistent with its original description (García, et al., 1986).

The male reproductive system in our specimens of R. aurata resembles the description of this organ by Gosliner (1990) for specimens from the Azores, but we could not observe a penial papilla. The seminal vesicle is shorter than in R. coronata and the atrium and male opening are broader ( Fig. 6A, B ). The female gland mass of R. aurata was never studied before and in our specimens of consists of one lobe, while in the studied specimens of R. coronata it is divided into two lobes ( Fig. 5B ).

The minimum uncorrected p -distance for the COI gene between R. coronata and R. aurata is 6.3% ( Table 3) and, in addition to the phylogenetic tree, the species delimitation analyses suggested both species as valid ( Fig. 2 ).

Figures

Figure 2. Runcina coronata species-complex. Detail of Clade F extracted from the analyses illustrated in Figure 1. Continuous rectangles, ABGD analysis based on the COI dataset. Dotted rectangles, bPTP analysis based on the COI dataset. *, branches with maximum support. 1, refers to sequences from Genbank.

Figure 3. Living animals of Runcina coronata (A, B) and Runcina aurata (C–F). A, MNCN 15.05/88105, 3 mm in length, Swanage (southern England). B, MNCN 15.05/90423, 4 mm in length, Swanage (southern England) (photos Ian F. Smith). C, MNCN/ADN 118948, 1.5mm in length, La Caleta, Cádiz (south-western Spain; Atlantic Ocean). D, MNCN/ADN 118950, 1mm in length, La Caleta, Cádiz (south-western Spain; Atlantic Ocean). E, MNCN 15.05/88106, 2 mm in length, La Caleta, Cádiz (south-western Spain; Atlantic Ocean). F, MNCN 15.05/88107, 2mm in length, La Caleta, Cádiz (south-western Spain; Atlantic Ocean). Photos A and B, courtesy of Ian F. Smith; photos C–F by Ana Karla Araujo.

Figure 4. Scanning electron micrographs of radula and gizzard plates. A–C, Runcina coronata. A, rachidian teeth (MNCN 15.05/88105). B, lateral teeth (MNCN 15.05/88105). C, gizzard plate (MNCN 15.05/90423). D–F, Runcina aurata. D, rachidian teeth (MNCN 15.05/91500). E, lateral teeth (MNCN 15.05/88106). F, gizzard plate (MNCN 15.05/88106). G–I, Runcina caletensis (MNCN 15.05/200113) G, rachidian teeth. H, lateral teeth. I, gizzard plate. J–M, Runcina tingensis. J, rachidian teeth (MNCN 15.05/200114). L, lateral teeth (MNCN 15.05/200114). M, gizzard plate (MNCN 15.05/91514). Scale bars: A, B, E, J, L = 10 μm; C, F, I, M = 50 μm; D, G = 20 μm; H = 5 μm.

Figure 5. Female reproductive system. A. R. coronata, southern England (MNCN 15.05/90423). B. R. aurata, La Caleta, Cádiz, south-western Spain, Atlantic Ocean (MNCN 15.05/88106). C. R. caletensis, La Caleta, Cádiz, south-western Spain, Atlantic Ocean (MNCN 15.05/200113). D.R. tingensis, Tangier, north-western Morocco,Atlantic Ocean (MNCN 15.05/91514). Abbreviations: FM, female mass; CGD, common genital duct; GO, gonopore.

Figure 6. Male reproductive system. A, Runcina coronata, southern England (MNCN 15.05/90423). B, Runcina aurata, La Caleta, Cádiz, south-western Spain, Atlantic Ocean (MNCN 15.05/88106). C, Runcina caletensis, La Caleta, Cádiz, southwestern Spain, Atlantic Ocean (MNCN 15.05/200113). D, Runcina tingensis, Tangier, north-western Morocco, Atlantic Ocean (MNCN 15.05/91514). Shaded area indicates the presence of sperm. Abbreviations: MO, male opening; PP, penial papilla; PG, prostate gland; SV, seminal vesicle.