Caribranchus morsomus (Marcus & Marcus, 1962)

Tibiriçá, Yara, Pola, Marta, Pittman, Cory, Gosliner, Terrence M., Malaquias, Manuel A. & Cervera, Juan Lucas, 2023, A Spanish dancer? No! A troupe of dancers: a review of the family Hexabranchidae Bergh, 1891 (Gastropoda, Heterobranchia, Nudibranchia), Organisms Diversity & Evolution (New York, N. Y.) 23 (4), pp. 697-742 : 721-726

Caribranchus morsomus (Marcus & Marcus, 1962) : Ortea et al. (2012: 24, Fig. 8D )

Distribution Caribbean: British Virgin Islands (Marcus & Marcus,), Puerto Rico (Marcus & Marcus, 1968), Guadeloupe (Ortea et al., 2012), Venezuela (Gutiérrez et al., 2015), Panama ( Collin et al., 2005), Costa Rica, Honduras, Aruba, Puerto Rico, St. Marteen/St Martin, St. Lucia, Martinique, Antigua, Grenada, St. Vincent and the Grenadines, Trinidad & Tobago (Valdés et al., 2006).

Material examined One specimen. CMPY000672 , length 44 mm (preserved), Arrecife Caro, Arenas, Yucatán, Mexico, collected by Deneb Ortigosa, 26 May 2017 .

External morphology ( Fig. 20 ) Commonly to 120 mm (with some reports to 200 mm). The body is oval. The examined specimen had a sub-pustulate to pustulate notum. Photographs of large mature, resting animals are usually strongly and evenly pustulate. The mantle is relatively wide, expanding and rolling on the sides and posteriorly, but not anteriorly. The mantle extends beyond the foot when expanded. The gills are compact and bushy with six tripinnate contractile (but non-retractable) gill branches distributed around an elevated anal papilla. The kidney pore is on the right side of the anal papilla. The gill branches are separated by thin tissue with two anterior branches clearly separated and four posterior branches arranged in pairs. The rhinophore is stocky and the club, in large mature animals, is relatively short with about 20 lamellae.

Ontogeny, color, and variation ( Fig. 20 ) No specimens or photos were available of very young juveniles. Nevertheless, Ortea et al. (2002) described an 8 mm specimen as white with a yellow edge, red rhinophores, and four white gill branches. Photographic material shows transitional animals to be white with variable red spotting on the pustules and a narrow red marginal line. With growth, the notum becomes mottled in red and cream. A broader, marginal red band with a straight and sharply defined inner margin develops on the dorsal surface. In large animals, the overall color darkens to red. The rhinophores are dark orange with white tips. Rhinophore lamellae may be sparsely flecked with white. The gills range from translucent red to translucent white with red lines on the rachis. The foot has a red margin.

As in other Hexabranchus spp. , during ontogeny, the mantle expands laterally and becomes rolled, the number of rhinophore lamellae increases, the gills become more elaborate, and the notum of resting animals assumes the mature texture.

Internal morphology Buccal mass ( Fig. 21 ). The radula is similar to the ones described by Marcus and Marcus (1968) and Valdés (2002) ( Fig. 21A–C ). Nevertheless, only a few traces of a triangular rudimentary rachis could be seen ( Fig. 21B ). It is unclear if this is an artifact of the condition of the radula, an ontogenetic character, or a variable feature. Radular formulae 40 × 88.0(?)0.88 ( CMPY 000672). Jaw deprived of rodlets ( Fig. 21D ).

Reproductive system ( Fig. 22 ) As described by Marcus and Marcus (1962).

Natural history and behavior Ortea et al. (2002) suggested that this species is an omnivore feeding on sponges, bryozoans, foraminiferans, and algae. According to them, the large oral tentacles are used to capture the high amount of food needed to supply the energy demands resulting from its large size and defensive swimming behavior. Other species of mottled, E mature, orange, F mature, red, G rhinophores, early transitional, H rhinophores, mature, I gills, light, J gills, dark, K oral tentacles, L swimming

Hexabranchus have been found with different stomach contents apart from sponges ( McDonald & Nybakken, 1997), but it is unclear whether or not they are accidental ingestions (Francis, 1980).

The examined specimen and online videos show that pustules on the notum tend to be less visible when the animal swims. The egg ribbon is relatively low, dull-red, and loosely coiled.

Remarks This species is distinguishable from all other species of Hexabranchus by the absence of jaw rodlets and the presence of a vestigial triangular rachidian tooth. Mainly because of this, Ortea et al. (2002) doubted that H. morsomus could have a common ancestor with other Hexabranchus spp. and proposed the genus Caribranchus to accommodate it. Nevertheless, the presence of a vestigial rachidian tooth is not a strong diagnostic character as it is often hard to see and may vary at species level (e.g., Hoover et al., 2017). The type of labial cuticle is usually a clearer character, but it may vary within a genus (e.g., Neuhaus et al., 2021). Moreover, our phylogenetic analysis reveals that the genus Hexabranchus is monophyletic and H. morsomus is the sister species to all Indo-Pacific species. The closest related species to H. morsomus is H. aureomarginatus , with an elevated genetic distance of 13.26% ( Table 3). They are easily distinguishable externally, but share a few similarities in the reproductive system, such as a female opening which appears to be visible in the genital atrium in both species, a loosely convoluted deferent duct (longer in H. aureomarginatus ), and a large, curved prostate.

Hexabranchus giganteus Tibiriçá, Pola & Cervera , sp. nov. ( Figs. 23 , 24 and 25 )

Zoobank Act. E9F31104-D3AD-409B-98AD-2614211B333A)

Material examined.

Holotype MHNM.MOL.2022.0001 (sequenced), length 380 mm, Ponta do Ouro , “The Cake”, Mozambique (26° 50′ 22″ S, 32° 54′ 39″ E), 36 m, 12 April 2022.

Paratype MB28-005009 (sequenced), length 110 mm, Ponta do Ouro , Atlantis, Mozambique (26° 50′ 58″ S, 32° 44′ 54″ E), 40 m, 16 July 2014 .

Other material MNCN: ADN 110938 (tissue), length 480 mm, Ponta do Atlantis , Mozambique (26° 50′ 58″ S, 32° 44′ 54″ E), 40 m, 16 April 2022 ; UL-YT1657 (dissected and sequenced), MNCN: ADN 110937 (tissue), length 430 mm, Nuarro , Nuarro Sacred Sands, Mozambique (14° 11′ 48″ S, 40° 59′ 18″ E), 04 Sep 2016 ; MNCN: ADN 110933 (tissue), length 420 mm, Ponta do Ouro , “The Cake”, Mozambique (26° 50′ 22″ S, 32° 54′ 39″ E), 42 mm, 23 July/2018 .

Etymology The specific name refers to the gigantic size of this species, one of the largest nudibranchs in the world.

Distribution Western Pacific and Western Indian Ocean. Red Sea (Yonow, 2008), Djibouti, Yemen ( Debelius, 1996), Mozambique (Tibiriçá et al., 2017), Seychelles, Madagascar ( Debelius & Kuiter, 2007), Tanzania ( Debelius, 1996), South Africa (pers. obs.), Hong Kong (Yonow, 2008), New Caledonia (Hervé, 2010), Indonesia (Tonozuka, 2003; Valdés, 2002), Papua New Guinea ( Colin & Arneson, 1995; Debelius, 1996), Japan (Nakano, 2018) including Okinawa ( Coleman, 2008). On-line sources: Oman, Philippines (iNaturalist), Emirates Arab (MedSlug), Mayotte (South-west Indian Ocean Seaslug site), Vanuatu (Underwater Australasia), and Fiji (Sea Slug Forum).

External morphology ( Fig. 23 ) Commonly up to 500 mm (with some reports to 700 mm in Madagascar). The notum of resting, mature animals is evenly pustulate (“quilted”). The body of mature animals is oval. The mantle is wide, expanding, and rolled on the sides and posteriorly (but not anteriorly). The foot extends slightly beyond the mantle. There are five to eight multi-pinnate gill branches separated in gill pockets. The anus is on an elevated papilla located in the center of the gill branches. The kidney pore is on the right side of the E mature, red, F mature, dark red, G mature, yellow, H notum detail, I unrolled mantle, J underside, K rhinophores, late juvenile, L rhinophores, mature, M gills, N oral tentacles, O laying eggs, P egg mass anus. The rhinophore clubs are elongate and slightly bent with approximately 80 lamellae (in large, mature individuals). The oral tentacles are large, fleshy, and elongated.

Ontogeny, color, and variation ( Fig. 23 ) No photos or specimens of very young juveniles were available but early transitional animals range from translucent gray to violet with orange rhinophores, orange gills with a cream rachis, a white marginal band, and a white rhinophore collar. Transitional animals develop diffuse pink spots on the notum. As the transition proceeds, the spots become sharply defined and darker pigment is deposited progressively outward from their boundaries filling the spaces between them (the process may not be fully complete until the animals reach 200–300 mm). As this happens, the notum becomes subpustulate and the rhinophores become yellow. In addition, reddish-pink patches appear on the underside of the mantle, on the mid-line of the “tail,” and on the lower portion of the rachis. Large animals may show thin, white, delicate lines that accentuate the pustulate appearance of the dorsum. In mature animals, the center of the notum is dark with lighter lozenges (corresponding to the diffuse pink spots of early transitional animals). The dorsal bands in mature animals are consistent in arrangement with a yellow marginal band, a dark submarginal band interrupted with elongate cream lozenges, and a yellow inner band. The background color is typically pink but varies from yellow to red. The gill rachis is cream grading to orange apically. The foot sole is yellow.

As in other Hexabranchus spp. , during ontogeny, the mantle expands laterally and becomes rolled, the number of rhinophore lamellae increases, the gills become more elaborate, and the notum of resting animals assumes the mature texture.

Internal morphology ( Fig. 24A ) The large, brown blood gland lies on top of the nerve ring. The light blue stomach is elongated and slightly wider than the intestine. The intestine passes between the reproductive system and digestive gland toward the elevated papillae anus. The gonad and digestive gland are cone-shaped, light brown, and bear light pink ducts.

Buccal mass ( Fig. 24 ) The radula (MNCN: ADN 110,933) is 23 mm long, broad, and bilobed (72 × 137.0.137). The anterior part of the radula is elevated ( Fig. 24A ). The lateral teeth are simple and hooked ( Fig. 24B ). The inner teeth are degenerate and triangular. The outer teeth are smaller

( Fig. 24C ). The jaw is smooth posteriorly with large and robust rodlets anteriorly (UL-YT1657, Fig. 24D ).

Reproductive system ( Fig. 25B–D ) Triaulic with the hermaphroditic duct leading to a very long, convoluted, pale pink ampulla. The ampulla passes between the female gland and the prostate gland, dividing into a short oviduct leading into the female gland mass and a deferent duct passing through the prostate portion. The prostate gland is granular, kidney-shaped, orange in color, stocky at its base, and narrowing toward the distal deferent duct. The distal deferent duct is thin and short leading to a muscular, thick portion. The deferent duct loops two to three times leading to the penial bulb that opens into a common atrium with the vagina. The vaginal duct curves once and then bifurcates, leadinvg to the dorsal side of the bursa copulatrix and to the receptaculum seminis. The receptacle seminal is very long, convoluted, pale pink, and located dorsally to the bursa copulatrix. The bursa copulatrix is black, large, and oval. The short uterine duct emerges between the receptaculum seminis and the bursa copulatrix, entering the female gland. The female gland is half-oval, pale-pink, granular, and smaller than the bursa copulatrix.

Natural history and behavior. This is the largest species of the genus Hexabranchus . Its behavior is largely unknown; individuals have been seen crawling on the reef during day and night. Though it is probably feeding primarily at night we observed mating and egg-laying during the day. The notum of resting mature animals is regularly subpustulate but the subpustules are reduced in prominence during swimming. It is most common in deeper water (usually over 30 m), but there are occasional reports as shallow as 15 m in the Indian Ocean and 5 m in the Pacific. The egg mass is salmon, densely folded, and slightly disorganized. The gills are held in a more erect position than in H. lacer and the sides of the genital papillae appear tapered in copulating pairs.

The swimming pattern of this new species (under the name H. sanguineus ) was studied using computational modelling and video by Zhou and Mittal (2017)

Figures

Fig. 8 Ontogeny, color, and variation in Hexabranchus sanguineus (lineage 1). Green circles indicate studied specimens and red online sources. A early transitional, pink, B mature, C unrolled mantle, red

Fig. 20 Ontogeny, color, and variation in Hexabranchus morsomus. Green circles indicate studied specimens and red online sources. A early transitional, B mid-transitional, C late transitional, D mature,

Fig. 21 Hexabranchus morso- mus (CMPY000672) radula. A General view, B central portion highlighting traces of rudimen- tary rachis, C outer teeth, D smooth jaws

Fig. 22 Hexabranchus mor- somus reproductive system. A Photography (CMPY000672), B reconstructed drawing. Abbreviations: amp, ampulla; bc, bursa copulatrix; dd, defer- ent duct; fmg, female gland; hd, hermaphroditic duct; p, penial bulb; pr, prostate; rs, receptacu- lum seminis; ud, uterine duct; v, vagina

Fig.23 Ontogeny, color, and variation in Hexabranchus giganteus sp. nov. Green circles indicate studied specimens and red online sources. A late juvenile, B transitional, C late transitional, D mature, orange,

Fig. 24 Hexabranchus gigan- teus sp. nov. (UL – YT1634). SEM photograph of the radula. A General view, B outer teeth, C inner teeth, D rodlets of the jaws

Fig. 25 Hexabranchus gigan- teus sp. nov. A Photography of internal anatomy of speci- men UL-YT1657 with details of the reproductive system (ventral view above and dorsal view below). B Reconstructed drawing. Abbreviations: amp, ampulla; bc, bursa copulatrix; bg, blood gland; dd, deferent duct; dg, digestive gland; fmg, female gland; h, heart; hd, her- maphroditic duct; it, intestine; p, penial bulb; pr, prostate; reps, reproductive system; rs, recep- taculum seminis; st, stomach, ud, uterine duct; v, vagina