Notobryon, Odhner, 1936

Pola, Marta, Camacho-García, Yolanda E. & Gosliner, Terrence M., 2012, Molecular data illuminate cryptic nudibranch species: the evolution of the Scyllaeidae (Nudibranchia: Dendronotina) with a revision of Notobryon, Zoological Journal of the Linnean Society 165 (2), pp. 311-336 : 317-323

GENUS NOTOBRYON

Synopsis of the genus Notobryon Odhner, 1936

Body sides smooth. Two pairs of dorsal lobes with long bases. Anus lateral, between the right lobes. Rhinophoral sheaths with an elevated posterior crest. Digestive gland divided into three compact masses (right, left anterior, and posterior). Radula without median tooth, rachis broad. Penis short, conical with flattened edge-shaped and bearing a small projecting lobe.

Type species: Notobryon wardi Odhner, 1936

NOTOBRYON WARDI ODHNER, 1936

( FIGS 1 , 2 , 3 , 4 , 5A–B )

Notobryon wardi Odhner, 1936: 1099 , plate 1, figures 1–3, text figures 31–38; Baba, 1949: 90, pl. 36, figures 131–132, text figure 114. Nakano, 2004: 217, bottom photo.

Notobryon sp. 1 Gosliner, Behrens &Valdés, 2008: 327, second photo from bottom.

Notobryon sp. 2 Gosliner, Behrens & Valdés, 2008: 327, bottom photo.

Type material: Lectotype (designated here): SMNH type no. 8092 Notobryon wardi Odhner, 1936 , east Australia, Queensland, Port Curtis, off Gatcombe Head , one adult specimen 58 mm preserved length, 16 m depth, vii.1929, leg. M. Ward and W. Boardman. The lectotype is intact and was not dissected in this study. Externally, it is in good condition but it is difficult to visualize a few features because the specimen is swollen or some structures are contracted, probably because of the preservation method . Paralectotypes (designated here): SMNH1346 , east Australia, Queensland, Port Curtis, off Gatcombe Head , three adult specimens 37, 50, and 51 mm preserved length (two specimens dissected), 16 m depth, vii.1929, leg. M. Ward and W. Boardman. Specimens with four labels, three of them handwritten by Odhner: one records ‘ Notobryon wardi n. gen. n. sp. Type, Det. Odhner’, the second records the number 4306, and the third one, ‘ Dredge off Gatcombe Head, Pt. Curtis about 9 f (illegible), July 1929. Coll. M. Ward & W. Boardman’. The fourth label corresponds to the printed label by the SMNH Museum with all the collecting information. Two of the three paralectotypes were dissected by Odhner. A vial inside the main container had one central nervous system, one complete jaw, two radulae, part of the buccal bulb, part of the stomach plates, and part of the digestive gland. One of the radulae was cleaned and mounted in a SEM stub by us. This is the radula that corresponds to the one that Odhner depicted in the original description. All these structures with the exception of the second radula belong to the 50 mm paralectotype specimen. The second radula remained inside the tissue and was also cleaned and mounted for SEM. In the 51 mm paralectotype, the labial cuticle was still inside the buccal bulb. All the internal organs are present except for the heart and radula. The stomach was opened to remove the stomach plates, the same one that we found in the glass vial. We counted seven plates in the stomach and we believe that one is missing and should be the one that was inside the vial. This plate was also mounted for SEM .

Other specimens: Papua New Guinea: CASIZ 075283 , Papua New Guinea, North coast, near Madang, inner side of barrier reef just south of Rasch Passage, Matthew’s Folly , 22 m depth, one adult specimen 15 mm preserved, dissected, 15.xi.1990, collected by (coll.) T . M. Gosliner , photo slide. CASIZ 086503 , Papua New Guinea, North coast, near Madang, inner side of Rasch Passage , 5 m depth, two immature specimens 5 & 10 mm preserved, dissected, 16.vi.1992, coll. T . M. Gosliner, photo slide. Indonesia: CASIZ 117360 , Indonesia, Banda Sea, Reong Island , out at night, 9 m depth, one adult specimen 35 mm alive (18 mm preserved), dissected, 3.xi.1998, coll. P. Fiene-Severns, photo slide. Hawaii: CASIZ 104662 , Hawaii, Maui, Makena , one immature specimen 13 mm alive, dissected, 19.v.1995, coll. P. Fiene- Severns, photo slide. CASIZ 101129 , Hawaii, Maui, Black Rock , 10 m depth, two immature specimens 5 mm preserved, 20.x.1994, coll. C. Pittman, photo slide. CASIZ 101109 , Hawaii, Maui, Airport Beach , on Halimeda , 9 m depth, one immature specimen 5 mm alive, 1.ix.1994, coll. C. Pittman, photo slide. CASIZ 105934 , Hawaii, Oahu, off Haleiwa , 109 m, two specimens 20 mm preserved (one dissected), date and collector unknown. CASIZ 116801 , Hawaii, Oahu, Kepuhi Point , exposed on rubble at night, 35 m depth, one specimen 20 mm preserved, 3.xii.1985, coll. S. Johnson, photo slide . Philippines: CASIZ 177589 , Philippines, Luzon Island, Batangas Province, Mabini, Mainit Bubbles , 16 m maximum depth, one adult specimen 20 mm preserved, dissected, 16.iv.2008, coll. T . M. Gosliner , digital pictures. CASIZ 177591 , Philippines, Luzon Island, Batangas Province, Mabini, Mainit Bubbles , 16 m maximum depth, one adult specimen 25 mm preserved, dissected, 16.iv.2008, coll. T . M. Gosliner , digital pictures. CASIZ 177759 , Philippines, Luzon Island, Batangas Province, Mabini, Mainit Bubbles , 17 m maximum depth, one adult specimen 25 mm preserved, dissected, 22.iv.2008, coll. T . M. Gosliner , digital pictures. CASIZ 177537 , Philippines, Luzon Island, Batangas Province, Mabini, Calumpan Peninsula , Mainit Bubbles , 23 m maximum depth, one adult specimen 20 mm preserved, 21.iii.2008, coll. T . M. Gosliner, A. Valdés, M. Pola, L. Witzel, B. Moore & A. Alejandrino, digital pictures. CASIZ 177540 , Philippines, Luzon Island, Batangas Province, Mabini, Calumpan Peninsula , Mainit Bubbles , 23 m max depth, one specimen 15 mm preserved, 21.iii.2008, coll. T . M. Gosliner, A. Valdés, M. Pola, L. Witzel, B. Moore & A. Alejandrino, digital pictures. Pacific Ocean: CASIZ 180378 , Marshall Islands: Kwajalein Atoll: South Loi Island: ‘ South Loi sandspit’, 8 m depth, one adult specimen 25 mm alive, 18.xi.2007, coll. S. Johnson, digital pictures .

Geographical distribution: Indo-West Pacific: originally described from Australia ( Odhner, 1936; Greer, 2000) this species is also found in the Philippines ( Köhler, 2001; Gosliner et al., 2008 identified as Notobryon sp.2 , present study), Papua New Guinea ( Coleman, 2008; Gosliner et al., 2008 identified as Notobryon sp.2 , present study), Japan ( Nakano, 2004), and Indonesia, Hawaii, and Marshall Islands ( Debelius & Kuiter, 2007; present study).

Etymology: This species was named after one of the collectors, M. Ward who collected the first four specimens by dredging in July 1929.

External morphology ( Fig. 1 ): The body is slender, soft, flaccid, and elevated but laterally compressed. There is a dorsal crest behind the posterior lobes that ends in a keel-like tail. The margin is continuous anteriorly to the narrowest point near the middle of the body. There are some additional more elevated parts, running towards and forming a marked crest on the elevated rhinophoral sheaths. The rhinophores are perfoliate with about ten to 20 lamellae. The front of the head is bilobed but without processes or tentacles. There are two pairs of dorsolateral lobes. These lobes are well developed, the first pair slightly larger than the posterior pair and nearly continuous at their bases leaving U-shaped spaces between them. Each dorsolateral lobe bears four delicately branched secondary gills on their upper surface that look like small trees, two on the inner surface of each lobe and two usually smaller ‘gills’ on the outer margin of each lobe. There are also one or two extra secondary tripinnate ‘gills’ located just in front of the posterior end of the foot. The anal papilla is located on the right side, between the two lobes. The genital opening is on the right side, beneath the anterior end of the first lobe. Minute holes or subcutaneous glands, whose function is indeterminate, cover the entire body.

The body surface is quite smooth and semitransparent or reddish-brownish but with fairly numerous small light blue spots, some coalescing into slightly larger blotches. There are also traces of light brown scattered all over the body surface. The secondary ‘gill’ stalks are mostly transparent but some have thin brown cores. Externally the ‘gills’ are sporadically scattered with shiny opaque white, usually near the bases.

Anatomy: The alimentary canal begins anteriorly with the buccal bulb that has a pair of elongate jaws that are somewhat brown and thickened along the masticatory process. The masticatory edge of the jaws is expanded into a wing-like flap ( Figs 2A , 3A ). Over the edge of this flap are a series of polygonal rodlets that have a series of denticles along their outer edge. These rodlets form a honey-comb pattern over the entire surface of the masticatory edge ( Figs 2B , 3B , 4A–B ). The radula is broad and lacks rachidian teeth ( Fig. 3C ). The radular formula of most of the dissected specimens is detailed in Table 1. The radula formula described by Odhner (1936) is 14 ¥ 22– 24.0.22–24. The formula of two of the syntypes is 12 ¥ 21.0.21. Each lateral tooth bore denticles on both sides ( Figs 2C–D , 3D–F , 4C–D ). The denticulation is usually stronger on the outer face of each cusp ( Fig. 3E–F ). The teeth gradually increase in size towards the outer margin except for the two to three outermost teeth. The salivary glands are a flocculent mass of fine branching tubules, surrounding the foremost part of the very wide oesophagus. The stomach is well developed and has thick folds on the walls forming a girdle of eight thick plate-like elevations, broadly triangular, with broad base and a central apex ( Fig. 3G ). The digestive gland forms three distinct unbranched lobes.

The reproductive system of two specimens is shown in Figure 5A–B . The ovotestis consists of two large and globular gonads lying on the upper side of the posterior liver mass. From each gonad a thin-walled duct passes forwards to the hermaphroditic duct. The distal end of the hermaphroditic duct gets wider and expands into a long and convoluted ampulla that branch into the vas deferens and the oviduct. The oviduct enters the female gland mass. The vas deferens is long, and somewhat folded. It lacks a morphologically well-differentiated prostate gland mass but about half of its length has a different texture and appearance. The remaining deferent duct is narrower and smoother ending in a dilated penis. The penis is a short conical shape with its external margin compressed into an edge ending in a triangular lobe with two short cups ( Figs 3H , 4E–F ). The vagina is short with an elongate and large bursa copulatrix.

NOTOBRYON BIJECURUM BABA, 1937

( FIGS 5C , 6A–D , 7 )

Notobryon bijecurum Baba, 1937: 166 figures 1–3; Baba 1949: 91, plate 37, figure 133, text figure 115. Nakano, 2004: 217, middle photo.

Material examined: CASIZ 089003 , Japan, Ryukyu Islands, Okinawa, 1.3 km east-north-east of Maekizaki, Seragaki Beach , 26°30.4′N, 127°52.6′E, mixed sand coral rubble, 40 m depth, one adult specimen 57 mm alive, dissected, 29.xi.1992, coll . R. Bolland, photo slide.

Geographical distribution: Currently known only from Japan ( Baba, 1937, 1949; Nakano, 2004; present study).

External morphology ( Fig. 6A–D ): The body is slender, soft, flaccid, and elevated, but laterally compressed. The foot is narrow. The posterior crest is moderately large with an entire margin. The rhinophoral sheaths have a posterior longitudinal crest. The rhinophores are perfoliate with 16 lamellae. The front of the head is expanded in a semicircular veil with a wavy margin. There are two pairs of dorsolateral lobes, the posterior ones are much smaller that the anterior ones. These lobes are nearly continuous at their bases leaving a U-shaped space between them. The margins of the dorsolateral lobes are entire. Each dorsolateral lobe bears four large and dendritic ‘gills’ on their upper surface and one on the tail. The anal papilla is located on the right side, between the two lobes. The genital opening is on the right side, beneath the anterior end of the first lobe.

The body surface is quite smooth, varying from transparent to semitransparent light orange or light yellow with bold opaque marking on the back and the sides. Sometimes there are small light blue spots, some coalescing into usually two larger blotches. The ‘gills’ are mostly transparent. Minute holes or subcutaneous glands of indeterminate function cover the entire body.

Anatomy: The alimentary canal begins anteriorly with a buccal bulb that has a pair of elongate jaws ( Fig. 7A ). The masticatory edge of the jaw-plate is formed into a wide flange closely covered with numerous scale-like armatures ( Fig. 7B ). The radula is broad and lacks rachidian teeth ( Fig. 7C ). The radula formula described by Baba (1937) for a 30 mm long specimen is 12 ¥ 14–16.0.14–16. The radula formula of the 57 mm specimen studied in this paper is 16 ¥ 24.0.24. Each lateral tooth bears denticles on both sides except for the first inner lateral tooth that lack any denticles ( Fig. 7D, E ). The teeth gradually increase in size towards the outer margin except for the last two outermost teeth that become smaller. The salivary glands are very elongate and flocculent surrounding the foremost part of the very long and narrow oesophagus. There are seven stomach plates that are thick and broadly triangular ( Fig. 7F ).

The reproductive system is shown in Figure 5C . The ovotestis is comprised of two large and globular gonad groups lying on the upper side of the posterior digestive gland mass. The anterior group is composed of four hermaphroditic glands whereas the posterior group consists of five hermaphroditic glands. The hermaphroditic duct expands into a wider and folded duct that functions as an ampulla. The ampulla branches into the vas deferens and the oviduct. The oviduct enters the female gland mass. The vas deferens has a morphologically well-differentiated prostate gland mass. The prostate is large and globular consisting of many small rounded glands ( Fig. 7G ). From the prostate continues a relatively short and folded duct that ends in a conical and pointed penis ( Fig. 7H ). The vagina is short and lacks a bursa copulatrix.

Figures

Figure 1. Notobryon wardi Odhner, 1936. Living animals. A, Australia, New South Wales, Port Stephens, photo by Ron Greer; B, Philippines, Luzon Island, Batangas Province, Anilao, Photo by T. M. Gosliner, CASIZ 177589; C, Philippines, Luzon Island, Batangas Province, Calumpan Peninsula, photo by T. M. Gosliner, CASIZ 177537; D, Marshall Islands, Kwajalein Atoll, South Loi Island, photo by J. Johnson, CASIZ 180378; E, Papua New Guinea, North coast, near Madang, photo by T. M. Gosliner, CASIZ 075283; F, Notobryon sp.B, Philippines, Luzon Island, Batangas Province, Anilao, Mainit Bubbles, photo by T. M. Gosliner, CASIZ 177759.

Figure 2. Notobryon wardi Odhner, 1936 (Paralectotype SMNH 1346), East Australia, Queensland. A, jaw, scale bar = 100 Mm; B, jaw elements, scale bar = 10 Mm; C, lateral teeth, scale bar = 30 Mm; D, detail of lateral teeth, scale bar = 20 Mm.

Figure 3. Notobryon wardi Odhner, 1936. Philippines specimens. A, CASIZ 177589, jaws, scale bar = 100 Mm; B, CASIZ 177589, jaw elements, scale bar = 1 Mm; C, CASIZ 177591, radula, scale bar = 100 Mm; D, CASIZ 177589, left rows of teeth, scale bar = 100 Mm; E, CASIZ 177589, central lateral teeth, scale bar = 20 Mm; F, CASIZ 177589, detail of a tooth, scale bar = 10 Mm; G, CASIZ 177589, stomach plates, scale bar = 100 Mm; H, CASIZ 177589, penis, scale bar = 100 Mm.

Figure 4. Notobryon wardi Odhner, 1936. Papua New Guinea (CASIZ 075283) and Indonesia (CASIZ 0117360) specimens. A, CASIZ 075283, jaw elements, scale bar = 1 Mm; B, CASIZ 0117360, jaw elements, scale bar = 2 Mm; C, CASIZ 075283, right rows of teeth, scale bar = 10 Mm; D, CASIZ 0117360, right rows of teeth, scale bar = 20 Mm; E, CASIZ 075283, penis, scale bar = 30 Mm; F, CASIZ 0117360, penis, scale bar = 20 Mm.

Figure 5. Reproductive system. A, B, Notobryon wardi Odhner, 1936. A, Paralectotype SMNH 1346; B, CASIZ 177589; C, Notobryon bijerecum Baba, 1837, CASIZ 089003; D, Notobryon thompsoni sp. nov., CASIZ 07400; E, Notobryon panamica sp. nov., MZUCR-INB0003118069; am, ampulla; bc, bursa copulatrix; fmgl, female gland mass; hd, hermaphroditic duct; p, penis; pb, penial bulb; pr, prostate; v, vagina; vd, vas deferens. Scale bar = 1 cm.

Figure 6. A–D, Notobryon bijerecum Baba, 1837, living animals. A, Japan, Ryukyu Islands, Okinawa, Seragaki Beach, photo by R. Bolland, CASIZ 089003; B, Japan, Shizuoka prefecture, photo by S. Yamamoto; C, Japan, Shizuoka prefecture, photo by T. Kurihara; D, Japan, Izu-Oshima Island, photo by H. Yamada. E-F, Notobryon clavigerum Baba, 1837, living animals. E, Japan, Fukui prefecture, photo by Y. Shamoto; F, Japan, Shizuoka prefecture, photo by A. Kawahara.

Figure 7. Notobryon bijerecum Baba, 1837, CASIZ 089003. A, jaws, scale bar = 100 Mm; B, jaw elements, scale bar = 1 Mm; C, radula, scale bar = 100 Mm; D, Inner lateral teeth, scale bar = 10 Mm; E, central lateral teeth, scale bar = 20 Mm; F, stomach plates, scale bar = 200 Mm; G, penis and prostate, scale bar = 100 Mm; H, penis, scale bar = 20 Mm.