Dendrodoris temarana Pruvot-Fol 1953

Dendrodoris temarana Pruvot-Fol 1953

Dendrodoris temarana Pruvot-Fol, 1953: 87–88, text fig. 31, pl. 3, fig. 55.

Dendrodoris limbata [non Cuvier (1804)]— Ballesteros (1978, 1984, 1985), García-Gómez (1984), Gómez-Álvarez (2017)

Dendrodoris grandiflora [non Rapp (1827)] —Valdés et al. (2016), Cyrne et al. (2018)

Dendrodoris herytra [non Valdés & Ortea in Valdés, Ortea, C. Ávila & Ballesteros (1996) in part] – Wirtz (1998), Cyrne et al. (2018)

Type material. The location of the holotype of Dendrodoris temarana is unknown, since the material examined by Pruvot-Fol (1953) was not deposited in any institution (P. Bouchet, pers. comm). One specimen collected from the type locality is designated as neotype herein.

Neotype. (Fig. 3A). Temara, Rabat-Salé-Kénitra, Morocco, (34º00’08.1”N 6º52’36.3”W) 30/03/2010, one specimen of 20 mm alive (pending number MNCN-15.05/200177; sequenced) col N. Tamsouri.

Additional material. Cape Ghir, Sus-Masa, Morocco, 27/04/2010 1 specimen 7 mm length preserved (pending number MNCN-15.05/94684; sequenced); 08/10/2009, one specimen 15 mm length alive (pending number MNCN-15.05/94683; sequenced); 22/06/2009, one specimen 8 mm length preserved (pending number MNCN-15.05/94682; sequenced), leg. N. Tamsouri; Cubelles, Catalonia, Spain, 05/04/2015, 1 specimen 17 mm length preserved (CRBA-92726; dissected); 30/06/2015, one specimen 40 mm length alive (CRBA-92721; sequenced) (Fig 3 C, D); one specimen 12 mm preserved (CRBA-92742; dissected and sequenced); 13/10/2015, two specimens 3 and 5 mm length preserved (CRBA-92730; dissected); six specimens 4, 4, 5, 5, 5 and 6 mm length (CRBA-92733; dissected); 13/11/2015, one specimen 5 mm length preserved (CRBA-92734; dissected); 14/12/2015, four specimens 7, 7, 8 and 11 mm length preserved (CRBA-92724; dissected); one specimen 37 mm length alive (CRBA-92737; sequenced) (Fig. 3E,F), one specimen 25 mm length alive (CRBA-92738; dissected and sequenced) (Fig. 3G,H); one specimen 19 mm length alive (CRBA-92741; sequenced); one specimen 38 mm length alive (CRBA-92743; sequenced); 15/02/2016, one specimen 33 mm length alive (CRBA-92744; sequenced); 14/03/2016, one specimen 12 mm length preserved (CRBA-92732; dissected); one specimen 25 mm length alive(CRBA-92739; sequenced); one specimen 35 mm length alive (CRBA-92740; sequenced); 18/04/2016, two specimens 17 and 27 mm length preserved (CRBA-92728; dissected), leg. C. Galià-Camps & M. Ballesteros; 29/10/2020, one specimen 18 mm length alive (SMF 360682) leg. M. Ballesteros; La Caleta, Cádiz, Andalusia, Spain, 02/11/2017, one specimen 23 mm length preserved (CRBA-92747; sequenced); one specimen 20 mm length preserved (CRBA-92735, sequenced); one specimen 17 mm length preserved (CRBA-92736, sequenced), leg. C. Galià-Camps; Gran Canaria, Canary Islands, Spain, 25/01/2017 one specimen 15 mm length preserved (CRBA-92745; sequenced); one specimen 14 mm length preserved (CRBA-92746; sequenced), leg. A. Herrero; Mitrena, Setúbal, Portugal, 20/04/2017, one specimen 26 mm length preserved (CRBA-92748; sequenced); Tróia, Setúbal, Portugal, 20/04/2017, one specimen 27 mm length preserved (CRBA-92749; sequenced), leg. G. Calado; Calhau, São Vicente, Cape Verde, 10/07/2013, one specimen 25 mm length preserved (MNCN- 15.05/200125, sequenced), leg. M. Pola & J. Reis. Serra Negra, Sal, Cape Verde, 05/04/2014, one specimen 9 mm length preserved (MNCN-15.05/92207, sequenced); Porto Cais, Maio, Cape Verde, 05/04/2007, one specimen 12 mm length preserved (MNCN-15.05/92208, sequenced); Estancinha, Boavista, Cape Verde, 04/2019, one specimen 10 mm length preserved (MNCN-15.05/92209, sequenced), leg. M. Jiménez & C.M. Alfonso.

External morphology. Live specimens up to 70 mm in length. Body elongated, posterior part of foot protrudes slightly behind mantle. Mantle soft without spicules, very wide relative to foot, smooth and wavy, slightly striated, generally lighter than rest of body. Juvenile specimens uniformly pale red, shifting to adulthood (Fig. S5). Adults with variable chromatic pattern; red, pinkish, yellowish, orange, dark brown or almost black (Figs. 3A, C, E, H). Uniform background color (usually in black or brown specimens) or with orange, reddish and brownish spots. Rhinophores with 15–20 oblique lamellae, same color as body, tips white (Fig. 3G). Rhinophoral sheaths with smooth edge, slightly raised above mantle. Gill with eight branchial leaves, two most posterior with common base (Figs. 3D, F). Rare cases of six (juveniles of 5–10mm), or 10 (largest specimens) branchial leaves observed. Gill with same color as mantle, sometimes darker, with lighter rachis, white apices. Anal papilla somewhat globose and prominent, with upper edge lobed. Ventrally, mantle margin, body flanks and foot with same color as the dorsum, lacking spots.

Internal anatomy. Buccal bulb small in relation to size of animal, surrounded by thin membrane with black dots. Esophagus with two folds (Figs. 4A, B). Intestine with numerous loops after emerging from the visceral mass proximally, becoming visible again between lobes of digestive gland (Fig. 4A, B). Ptyalin gland yellowish, located below folds of esophagus; highly developed and divided into two main lobes, composed of smaller lobes (Fig. 5A, B). Ptyalin gland joined to buccal bulb, anterior to nervous esophageal collar. Digestive gland brown, lobulated, occupying posterior half of visceral mass. A lobe of digestive gland located posterior to reproductive system (Fig. 4B). Central nervous system posterior to buccal bulb. Heart, surrounded by pericardial membrane, located on posterior lobe of digestive gland. Aorta directed forward, running over organs of visceral mass. Blood gland brown, left of anterior region of aorta (Figs. 4A, B). Hermaphroditic gland granular, lobed, yellowish, occupying central part of visceral mass (Fig. 5C, D). Rest of reproductive system in anterior right area of visceral mass. Female gland complex well developed with distinct mucus gland posteriorly. Ampulla folded with at least three folds under prostate. Bursa copulatrix between ampulla and prostate, 3–4 times larger than seminal receptacle. Prostate long, thick, granular, profusely folded on itself. Vas deferens with sinuous proximal portion, straight distally. Penial hooks small, with elongated base seen by transparency (Fig. 6).

Habitat and biology. Dendrodoris temarana is found under stones from the intertidal zone to several meters deep. In Cubelles, Catalonia, the species is common and has been documented for forty years in shallow waters (0–1 m deep) under boulders. Groups of 3– 5 specimens can be found gathering under the same stone. Visual censuses carried out in the 1980s reported up to 40 specimens per hour of sampling (MB pers. obs.). In Cádiz, D. temarana is the most abundant nudibranch, co-occurring with D. grandiflora, much less abundant, under exposed stones at low tide (pers. obs.). Egg masses are laid under stones and are 8 mm wide, ivory-colored ribbons, coiled into a spiral with several whorls, which can reach 5 cm in total diameter (Fig. 3B). There are usually 60– 70 eggs across the width of the ribbon, arranged in two superposed layers. The eggs have a diameter of about 80 µm and are enclosed in larger capsules of approximately 140 μm in diameter. Egg laying has been observed from May to November (JLC, MB, pers. obs.).

Geographic distribution. Dendrodoris temarana ranges from western Mediterranean Sea, South Portugal, Morocco, Canary Islands and Cape Verde (Fig. 7). In Catalonian coast (NE Spain) and Cádiz (Andalusia, SW Spain) it is very abundant. Recorded from El Portil (SW Spain) (García-Gómez 1984), Gulf of Cádiz (Gómez-Álvarez 2017) and Cubelles (Ballesteros 1978, 1984, 1985) as D. limbata. Records from the Portugese mainland (Cyrne et al. 2018), the Azores (Wirtz 1995, 1998) and the Canary Islands (Valdés et al. 1996) were misidentified as D. herytra. This species was also misidentified as D. grandiflora in Portugal (Cyrne et al. 2018), the Canary Islands (Valdés et al., 1996), Agadir (Valdés et al. 1996), and Mauritania (Valdés et al. 1996). Photographs or video records corresponding to Dendrodoris temarana from Thau (SE France), Ebro Delta (NE Spain), the Balearic Islands (E Spain), and La Línea de la Concepción (S Spain) are available from various internet websites (Suppl. Table 1).

Remarks. Dendrodoris temarana was described by Pruvot-Fol (1953) based on six specimens collected by Hélène Gantés and Jean B. Panouse in the town of Temara, on the Atlantic coast of Morocco. The only illustration of the living specimens of the original description is a color drawing made by Gantés which appears in Pruvot-Fol (1953, pl. 3, fig 55). Thanks to this drawing and the original description of the internal morphology we have been able to recognize the unidentified Atlantic-Mediterranean specimens recovered in the phylogenetic and species delimitation analyses as D. temarana. Since the original type material was never deposited (Bouchet, Gofas, pers. com.) and its location is unknow, a neotype collected in Temara (Morocco) is hereby designated to fix the taxonomic status of this species, which is often confused with Dendrodoris grandiflora as well as with Dendrodoris herytra and Dendrodoris limbata. The designation of a neotype is therefore consistent with Article 75 of the ICZN (1999) as there is an exceptional need to clarify the status of this species. The neotype closely resembles the external morphology of the original description by Pruvot-Fol (1953, pl. 3, fig 55) (Fig. 3).

Dendrodoris temarana can be distinguished from the other Dendrodoris species from the Atlantic and Mediterranean Sea by its chromatic pattern, since it is the only species that has bright colorful background patterns ranging from yellow to reddish (Fig 3A, C, E) or even black (Fig 3H), as observed by Pruvot-Fol (1953) in some of its preserved specimens, as well as the absence of patches on the foot and internal differences in the digestive and reproductive systems. Dendrodoris temarana has been misidentified as D. grandiflora (Valdés et al., 1996) and D. limbata (Ballesteros 1978), however, in D. grandiflora the dorsum is pale grey with brownish and black patches (Valdés et al., 1996. fig 1C), with some spots on the lateral side of the foot, while the dorsum of the dark morphotype of D. temarana has no patches and the foot is totally patchless (Table 3). Specimens of D. limbata can have colorful backgrounds, with well-delineated dark dorsal patches and a clear yellow-orange wide band on the perimeter of the body (Valdés et al., 1996. fig 1A, B). Dendrodoris temarana can be distinguished from D. limbata because it has a brighter color pattern, diffuse patches on the dorsum and lacks the yellow margin (Table 3). Moreover, specimens of D. limbata have numerous dark spots on the foot and the flanks of the body ventrally, while specimens of D. temarana have a uniform ventral color, without spots. When compared to NE-Atlantic Dendrodoris species, D. temarana is easily distinguishable from D. herytra, which has a uniform orange to reddish notum without patches and a small gill. Black colored D. herytra individuals reported by Valdés et al. (1996) are misidentifications of D. temarana, which has a broad color spectrum.

Dendrodoris temarana possess several morphological similarities to D. senegalensis, a species with which is partially sympatric (Table 3). The only external trait which may distinguish D. temarana and D. senegalensis is the size of the dorsal patches, larger in D. senegalensis. Nevertheless, internal anatomy features are much more reliable to differentiate these two species since D. temarana has two folds in the esophagus (Fig. 5A) and D. senegalensis has three of them (Valdés et al. 1996, fig 9). Moreover, their reproductive systems are clearly different, with D. temarana having a female gland as large as the prostate and three folds in the ampulla (Figs. 5C–D), while the female gland of D. senegalensis is 3–4 times as large as the prostate and the ampulla has two folds (Valdés et al. 1996, fig 9). Also, the deferent duct and vagina of D. senegalensis are folded several times (Valdés et al., op. cit.), while they are long and straight with a fold at the proximal end in D. temarana. The shape of the penial hooks is also different, having elongated bases in all of the hooks of D. temarana (Fig. 6), while this is not the case in D. senegalensis (Valdés et al., 1996, fig 9). The egg masses are also different, white in D. temarana (Fig. 3B) and yellow and narrow in D. senegalensis (Table 3). Finally, D. temarana is morphologically similar to the Caribbean species D. krebsii. However, these two species can be externally distinguished by the gill size, large in D. temarana but smaller in D. krebsii. Internally, D. krebsii differs from D. temarana because its esophagus has four folds, the ampulla has only one-fold, and the vagina and vas deferens have at least two folds (Valdés et al 1996, fig 7); moreover, the egg mass of D. krebsii is yellow, with small egg capsules (85 μm) (Valdés et al. 1996) compared to those of D. temarana (140 μm) (Table 3).

Two other species described by Pruvot-Fol, Dendrodoris pseudorubra Pruvot-Fol, 1951 and Dendrodoris longula Pruvot-Fol, 1951 are possible synonyms of D. temarana. However, due to the lack of information in these descriptions, we are unable to confirm their identity, and therefore we consider Dendrodoris temarana as the valid species name.