Goniobranchus preciosus (Kelaart, 1858)

Soong, Giun Yee, Bonomo, Lynn J., Reimer, James D. & Gosliner, Terrence M., 2022, Battle of the bands: systematics and phylogeny of the white Goniobranchus nudibranchs with marginal bands (Nudibranchia, Chromodorididae), ZooKeys 1083, pp. 169-210 : 169

Goniobranchus preciosus (Kelaart, 1858)

Figures 2c-f , 5c, d , 8a-f

Doris preciosa Kelaart, 1858: 98; 1883: 89.

Chromodoris preciosa : Eliot 1906: 642-643, pl. XLII, fig. 3; Eliot 1909: 92---93; Gosliner et al. 2008: 219, lower left and lower right photographs.

Goniobranchus preciosus : Gosliner et al. 2015: 222, lower left and lower right photographs; Gosliner et al. 2018: 152, lower left and lower right photographs.

Type locality.

Sri Lanka (as Ceylon), Indian Ocean.

Type material.

Most likely lost to science. Eliot (1906) refers to a few of Kelaart’s specimens being present in the collections of the Hancock Museum (now the Great North Museum) and that many of these specimens are useless for taxonomy. A search of the collections online indicates that no specimens of Doris preciosa are currently held in their collection. We made comparisons to Kelaart’s original drawings and description (Kelaart, 1858), as well as to updates by Eliot (1906, 1909) and Rudman (1985).

Geographical distribution.

Widely distributed around the tropical and subtropical Indo-Pacific oceans ( Rudman 1985; Debelius and Kuiter 2007; Coleman 2008; Gosliner et al. 2008, 2015, 2018) with specific reports from Sri Lanka ( Kelaart 1858), west coast of India and the Andaman Islands ( Kumar et al. 2019), Thailand ( Mehrotra et al. 2021), Philippines, Indonesia, Malaysia ( Gosliner et al. 2008), and Japan ( Nakano 2018; Ono and Katou 2020). Records cited by Gosliner et al. (2008) from New Caledonia, Tonga, Fiji, Vanuatu, and Australia are of Goniobranchus fabulus sp. nov., not G. preciosus .

Material examined.

CASIZ 208420 (morphotype A), one specimen (10 mm preserved), subsampled for molecular data, sand slope with reef, 13.522°N, 120.947°E, Manila Channel , Puerto Galera , Oriental Mindoro Province, Mindoro , Philippines, 4-22 m depth, 11 April 2015, T.M. Gosliner 2015 Verde Island Passage Expedition. CASIZ 208415 (morphotype A), one specimen (9 mm preserved), subsampled for molecular data and dissected, School Beach, 13.517°N, 120.950°E, Batangas Channel, Puerto Galera, Oriental Mindoro Province, Mindoro, Philippines, 18 m depth, 10 April 2015, T.M. Gosliner 2015 Verde Island Passage Expedition. CASIZ 208574 (morphotype B), one specimen (11 mm preserved), subsampled for molecular data and dissected, School Beach, 13.516°N, 120.950°E, Batangas Channel, Puerto Galera, Oriental Mindoro Province, Mindoro, Philippines, 6-17 m depth, 8 April 2015, T.M. Gosliner 2015 Verde Island Passage Expedition. CASIZ 176752 (morphotype C), one specimen (10 mm preserved), subsampled for molecular data, Pulau Gut, 2.664°N, 104.167°E, Pulau Tioman, South China Sea, Peninsular Malaysia, 13 m depth, 4 October 2007, T.M. Gosliner. CASIZ 176761 (morphotype D), one specimen (9 mm preserved), subsampled for molecular data, Tiger Point, 2.889°N, 104.061°E, Pulau Tioman, South China Sea, Peninsular Malaysia, 17-19 m depth, 2 October 2007, T.M. Gosliner .

Description.

External morphology. Living animal approximately 15 mm in length. Body white, with low tubercles on the notum; oval and elongated, with three marginal bands on the mantle edge. There is an outermost blue band followed by a deep red submarginal band and a yellow inner submarginal band. Brownish or orange dorsal spotting may be present over the surface of the mantle. In all cases the rhinophores are translucent reddish brown with white edges on the lamellae. The same pigment extends below the rhinophore club onto the stalks of the rhinophores. Rhinophore lamellae number 12-17. Gill branches reddish brown with white lines on the rachis. Nine or ten unipinnate gill branches held erectly when the gill is fully extended. This species exhibits four distinct morphotypes in addition to the unvarying elements described above. Morphotype A (Fig. 2c ) has a translucent creamy white body with fine orange spots and blotches on the notum. The outermost portion of the mantle edge is surrounded by a thin opaque bluish white band, followed by a thicker deep red band and then a yellow-orange submarginal band. Gill and rhinophores are translucent red with white edges. Morphotype B (Fig. 2d ) has a translucent pale yellow body with brown spots and blotches on the notum. The outermost portion of the mantle edge is surrounded by an opaque bluish white tinged band, followed by an irregular deep red and a yellow-orange submarginal band, with all three bands having similar widths. The gill and rhinophores are translucent brown with opaque cream edges. Morphotype C (Fig. 2e ) has an opaque white body with a few low tubercles. The outermost portion of the mantle edge is surrounded by a thin, opaque, bluish white band, followed by thicker deep red and yellow-orange bands. The gill and rhinophores are translucent red with opaque white edges. Morphotype D (Fig. 2f ) has a creamy white translucent body with densely speckled orange spots on the notum. The outermost portion of the mantle edge is surrounded by a thin opaque bluish white tinged band, followed by irregular deep red and yellow-orange bands, all three bands having similar widths. The gill and rhinophores are translucent red with opaque white edges.

Buccal mass and radula (morphotype B). The muscular portion of the buccal mass is ~ 2 × the size of the oral tube length (Fig. 5c ). The chitinous labial cuticle is found at the anterior end of the muscular portion of the buccal mass, bearing long, bifurcated jaw rodlets (Fig. 8a, b ). The radular formula of CASIZ 208574 is 54 × 47.1.47 (Fig. 8c ). The rachidian tooth has a flame-like shape and is blunt at the tips. The inner and outer surfaces of the inner lateral teeth have three or four denticles on each side of the central cusp (Fig. 8d ). The central cusp on the inner lateral tooth is ~ 2 × the length of the adjacent denticles. The middle lateral teeth have a long central cusp with 5-8 denticles (Fig. 8e ). The outer lateral teeth are rounded and paddle-shaped with six or seven denticles (Fig. 8f ).

Reproductive system (Fig. 5d ). The thick, tubular ampulla narrows into a diverging short oviduct and long vas deferens. The proximal prostatic portion of the vas deferens is narrow and convoluted, then transitions into an equally thin muscular ejaculatory portion. The narrow ejaculatory portion elongates into a wider section and again narrows prior to entering the short penial bulb, which joins with the distal end of the vagina. The vagina is short and moderately wide. It terminates at the junction of the large, spherical bursa copulatrix, the curved, pyriform receptaculum seminis, and the uterine duct. The long narrow uterine duct emerges from junction of the vagina, bursa copulatrix, and the receptaculum seminis and enters into the female gland mass. The female gland mass has small albumen and membrane glands and a large mucous gland.

Remarks.

Rudman (1985) redescribed specimens of G. preciosus from New Caledonia based on the description by Kelaart (1858) and the illustration in Eliot (1906) from Sri Lanka (as Ceylon). Rudman stated that Eliot’s (1906) reproduction of Kelaart’s drawing of Doris preci os a did not match the original description of G. preciosus by Kelaart (1858). However, Kelaart’s written description and the reproduction of his drawing by Eliot (1906) clearly match the three main morphotypes of G. preciosus found in this study. Additionally, Eliot (1909) reported on another G. preciosus specimen collected by Willey in Sri Lanka that had a few obscure spots on its notum, but Eliot’s notes did not mention any light bluish tinge on the outermost mantle edge. Rudman (1985) doubted that Eliot’s (1909) specimen was the real G. precio s us due to these few obscure spots and the absence of a light bluish margin. Hence, Rudman (1985) considered his specimen from New Caledonia as G. preciosus based on the descriptions from both Kelaart and Eliot. However, Rudman’s specimen lacks the dense red spotting described by Kelaart, but illustrated by Eliot, and that is present in the specimens studied here. Eliot’s illustration matches G. preciosus morphotype A found in this study. Based on the phylogenetic data in this study, the morphotype that matches Kelaart’s description (morphotype D; Fig. 2f ) and the morphotype that matched Rudman’s description ( G. fabulus sp. nov.; Fig. 4a-c ) are clearly distinct from each other. This distinction, as well as the fact that the species that Rudman identified as G. preciosus is not found in the Indian Ocean and appears to be restricted to the Western and Central Pacific, suggest separate species and Rudman’s G. preciosus is herein described as G. Goniobranchus fabulus sp. nov. These species have been frequently confused and often considered as a single species (e.g., Gosliner et al. 2018), but there are clear morphological distinctions as found in this study. In G. preciosus , the mantle always has some low tubercles, whereas the notum is smooth in G. fabulus . The gill branches of G. preciosus are more erect than those of G. fabulus . The gill and rhinophores of G. precious are reddish brown, whereas they are reddish purple in G. fabulus . In G. precious the club and stalk of the rhinophores have reddish pigment whereas in G. fabulus only the rhinophore club is pigmented and the stalk is the same white as the body. The two species overlap in the Philippines (present study), but G. preciosus is found north and westwards from the Philippines and G. fabulus is found to the south and eastwards from there.

Goniobranchus preciosus was recovered as a distinct species in the phylogenetic and ABGD analyses and was sister to a clade containing G. daphne (interspecific p -COI distances between G. preciosus and G. daphne = 7.4-7.9%; Table 2 ), Goniobranchus fabulus sp. nov. (interspecific p -COI distances between G. preciosus and G. fabulus sp. nov. = 6.8-9.2%; Table 2 ), and G. sinensis (interspecific p -COI distances between G. preciosus and G. sinensis .= 7.1-9.8%; Table 2 ). Goniobranchus preciosus has a high level of intraspecific morphological diversity with the presence of four morphotypes confirmed in this study and yet showed little genetic difference (intraspecific distance within G. preciosus = 0.4-2.7%; Table 2 ). These four morphotypes have very close external morphological similarities with G. verrieri morphotype B and G. sinensis , with all of them having three marginal bands on the mantle edge and with G. verrieri morphotype B and some morphotypes of G. sinensis having spots and patches on the notum. However, G. verrieri morphotype B has a greatly reduced outer white band compared to the much wider bluish bands of G. preciosus and G. sinensis . Only very subtle external morphological differences separate G. preciosus from the other species in this study. Goniobranchus preciosus morphotype A has a deeper red submarginal band while G. verrieri morphotype B has a paler red submarginal band. Goniobranchus preciosus morphotype B has a pale yellow body coloration that was not observed in any other specimens in this study. Goniobranchus preciosus morphotype C is very similar to G. fabulus morphotype A and G. sinensis morphotype C; however, the gill and rhinophore colors are not the same: G. preciosus has translucent red rhinophores and gills with opaque white edges, G. fabulus morphotype A has reddish purple rhinophores and gills with opaque white edges, and G. sinensis morphotype C has translucent red rhinophores and gills with opaque reddish purple edges. Goniobranchus preciosus morphotype D has densely speckled orange spots on the notum and an opaque bluish white tinged band on the mantle edge and this character combination was not observed in any other specimens in this study. Goniobranchus preciosus morphotype D also most closely matched the original external morphology of G. preciosus as described by Kelaart (1858).

With regards to internal morphology, G. preciosus and G. sinensis each have a flame-shaped rachidian tooth, but differ in their external colors and morphologies. Goniobranchus preciosus has a tuberculate body texture, whereas G. sinensis has a smooth notum. The rhinophores of G. preciosus are reddish brown and have spots of the same color extending onto the rhinophoral stalk. In G. sinensis , the rhinophores have reddish purple edges along the lamellae of the club and solid reddish purple rather than scattered spots extending onto the rhinophore stalk. Both species have three marginal bands which are similar in color but in G. preciosus the innermost band is more yellow-orange whereas it is more yellow in G. sinensis . These differences in color are subtle but appear to be consistent in the specimens studied here.

The high morphological diversity of G. preciosus suggests two different forms of morphological adaptations. Goniobranchus preciosus had different color patterns within the same locality, with two different morphotypes occurring both in the Philippines and in Peninsular Malaysia. At the same time, from a regional perspective, G. preciosus had color patterns specific to each locality. This is not the first time such a situation has been observed in nudibranchs, as previous studies have demonstrated a form of mimicry in chromodorid nudibranchs resulting in certain chromodorid species displaying morphological variation within a locality as well as individuals with same color pattern within the same locality turning out to be different species ( Padula et al. 2016; Layton et al. 2018, 2020).

Figures

Figure 2. a, b Goniobranchus albonares a CASIZ 191440, Papua New Guinea b CASIZ 228939, Philippines c-f Goniobranchus preciosus c CASIZ 208415, Morphotype A, Philippines d CASIZ 208574, Morphotype B, Philippines e CASIZ 176752, Morphotype C, Peninsular Malaysia f CASIZ 176761, Morphotype D, Peninsular Malaysia g, h Goniobranchus rubrocornutus g CASIZ 203047, Morphotype A, Philippines h CASIZ 208563, Morphotype B, Philippines. Photographs TMG. Scale bars: 1 cm.

Figure 4. Goniobranchus fabulus sp. nov. a CASIZ 177517, morphotype A, Philippines b CASIZ 177685, morphotype A, Philippines c CASIZ 201949, morphotype A, Philippines d CASIZ 191118, morphotype B, Papua New Guinea. Photographs TMG. Scale bars: 1 cm.

Figure 5. a buccal mass of Goniobranchus albonares, CASIZ 228939 b reproductive system of Goniobranchus albonares, CASIZ 228939 c buccal mass of Goniobranchus preciosus, CASIZ 208574 d reproductive system of Goniobranchus preciosus, CASIZ 208574 e buccal mass of Goniobranchus rubrocornutus, CASIZ 203047 f reproductive system of Goniobranchus rubrocornutus, CASIZ 203047. Abbreviations: am, ampulla; bb, buccal bulb; bc, bursa copulatrix; ej, ejaculatory duct; es, esophagus; fgm, female gland mass; ot, oral tube; p, penis; pr, prostate; ra, radular sac; rs, receptaculum seminis; va, vagina; mu, mucous gland. Scale bars: 0.1 mm (a, b, e, f); 1 mm (c, d).

Figure 8. Scanning electron micrographs. Goniobranchus preciosus, CASIZ 208574, Philippines a jaw b jaw rodlets c radula d central teeth e mid-lateral teeth f outer lateral teeth.