Paradoris liturata

Dayrat, Benoît, 2006, A taxonomic revision of Paradoris sea slugs (Mollusca, Gastropoda, Nudibranchia, Doridina), Zoological Journal of the Linnean Society 147 (2), pp. 125-238 : 188-195

PARADORIS LITURATA ( FIGS 17D–H , 45–51 )

Discodoris ? liturata Bergh, 1905: 106–107 , plate XIV, figs 15–20.

Discodoris ? liturata var. Bergh, 1905: 107, plate XIV, fig. 21. New synonym.

Paradoris liturata . – Dayrat & Gosliner, 2005: 201– 203, 206–209, 218, 219, 223.

Type material: Holotype of liturata , by monotypy: probably lost; it is neither at the ZMA (with the rest of the material from the Siboga expedition) nor at the ZMUC (with the rest of Bergh’s own material). According to the original description, the type locality of liturata is station 315 of the Siboga expedition. According to the list of stations of this expedition, this station is: 07°36′S, 117°30.8′E, anchorage, east of Sailus Besar, Paternoster Islands [also called Pulu Tenga], up to 36 m depth, dredge, 17/ 18 February 1900.

Holotype of liturata var., by monotypy: probably lost; it is neither at the ZMA (with the rest of the material from the Siboga expedition) nor at the ZMUC (with the rest of Bergh’s own material). According to the original description, the type locality of liturata var. is station 164 of the Siboga expedition. According to the list of stations of this expedition, this station is: 01°42′S, 130°47.5′E, Sele (Galewo-)Strasse [strait between Pulu Salawati and Pulu Misool, at the northwestern end of Irian Jaya, Indonesia], 32 m depth, dredge, 20 August 1899.

Additional material dissected: Papua New Guinea, Solomon Sea, Louisiade Archipelago, Calvados Chain , Rawa Reef , Yuma Passage , Snake Channel , east side of Yuma Passage between Tagula and Yejna Islands, 11°22.14′S, 153°20.99′E, 3 June 1998, one specimen 16/ 10 mm preserved, leg. Marty Fenton, identified as D. liturata by T. M. Gosliner ( CASIZ 113658 ) ; Papua New Guinea, north coast, Madang, slope off ‘ Madang Resort’ , 20 m depth, 4 August 1989, one specimen 12/ 5 mm preserved, leg. M. T. Ghiselin, identified as D. liturata by T. M. Gosliner ( CASIZ 069612 ) ; INDO- NESIA, North Sulawesi, Lembeh Strait, Serena Island , 3 November 1993, two specimens 35/14 (#1) and 27/14 (#2) mm preserved, leg. Pauline Fiene, identified as D. liturata by T. M. Gosliner ( CASIZ 097595 ) .

Type locality: Indonesia. Distribution: Papua New Guinea (present study), Indonesia ( Bergh, 1905, as liturata and liturata var.; present study).

Occurrence: So far, liturata is only known from six specimens (four specimens studied here and two types). A photograph of a live animal was found in the CASIZ pictures collection (Tabat Island, Papua New

Guinea, 1988, T. M. Gosliner), but the specimen itself could not be found.

Habitat: Sand, small stones and shells (Siboga station 164, liturata var.), coral and lithotamnion bottom (Siboga station 315, liturata ). No information was available for the additional material.

Remarks on the original description of liturata ( Fig. 17D ): The original description of liturata was based on a single specimen that was 14 mm long and 7 mm wide, certainly preserved. The dorsal notum was described as ‘black’ with an irregular number of ‘white plumps of 0.5 mm in diameter’ indistinctly arranged in four rows. The greyish mantle margins had discon- tinuous, radiating, quite wide bars ( Fig. 17D ). Bergh (1905) did not mention the number of rhinophoral lamellae. The five gills were greyish-white. At the end of the description, Bergh wrote that liturata was characterized by having a Phylidiella -like dorsal colour. Concerning the general morphology, Bergh described the shape of the animal as ‘long-oval, the back a little bit arched’. However, he did not mention whether the anterior foot was bilabiate and with a notched upper lip. Nor did he mention whether the digitiform oral tentacles were grooved. According to Bergh, the consistence was ‘not hard, but a little bit stiff ’. Bergh did not describe any holes on the surface of the dorsal notum. The labial cuticle was described as ‘strong, yel- low’ with plates ‘whose elements were 0.08 mm long and had a free bent tip of a height of 0.025 mm’. However, Bergh did not mention the exact number of jaw plates. Bergh mentioned a radular formula of 79 × (20- 0-20) and represented some lateral teeth that can be interpreted as grooved. Bergh’s drawings, however, do not allow us to determine the morphology of the outermost lateral teeth. The description of the reproductive system was exceptionally brief: ‘whitish and brown-yellow genital mass in front; penis unarmed’. Bergh’s description of liturata , which is much shorter (about one page long) than Bergh’s usual descriptions, is largely incomplete and ambiguous. It is probable that Bergh simply forgot to mention several important features. In that regard, some characters can be used as indicators of other characters: for example, the presence of digitiform oral tentacles strongly suggests that the anterior notum was bilabiate with a notched upper lip.

Remarks on the original description of liturata var.: The original description of the variety of liturata was extremely brief, and based on a single specimen that was 22 mm long and 13 mm wide, certainly preserved. Bergh (1905) distinguished this specimen as a variety of liturata because some white plumps over the black dorsal notum were larger (4 mm in diameter) than in the type of liturata (0.5 mm). Bergh actually pointed out that the Phylidiella -like pattern of the notum was more obvious in the variety than in the typical form. In addition, Bergh indicated that the radula and the jaws were similar to the typical form. However, he could not give any other anatomical details because of the poor condition of the specimen.

Description of new specimens ( Figs 45–51 ): The ground colour of the dorsal notum of live animals is light greyish, almost whitish ( Figs 17E–H , 45A, B ). It bears a network of wide, continuous black lines. The number and the positions of these black lines vary among individuals: only three longitudinal lines ( CASIZ 113658); three longitudinal and several transversal lines ( CASIZ 069612, CASIZ 097595 #2); or a complicated network of both longitudinal and transversal lines. In two specimens ( CASIZ 069612, CASIZ 097595 #1), the margin of the notum bears some lines radiating from the centre; those lines, not conspicuous, may be absent when preserved ( CASIZ 113658). The dorsal notum also bears white plumps of various sizes surrounded by the network of black lines. The rhinophores are dark grey. The gills are grey, but their darkness varies. Overall, despite the variation, the colour of the dorsal notum mimics Phylidiella. This pattern is still distinguishable after preservation ( Figs 45A, B ), more exactly after 10 years of preservation, but we do not know how these specimens will be in 100 years.

The body is oval, elongated ( Fig. 17E–H ). The largest specimens are 35 mm long preserved, i.e. approximately 40–45 mm long alive ( CASIZ 097595 #1). The foot is rounded posteriorly and anteriorly. The width of the foot equals approximately one-third or one-half of the width of the dorsal notum (in preserved specimens). The anterior margin of the foot is bilabiate and the upper lip is notched ( Fig. 45D ). The oral tentacles are grooved and digitiform ( Fig. 45D ). The dorsal notum bears plumps of different sizes. These plumps are not indecora -like ( Figs 17E–H , 45A, B ). They are much larger. Despite the presence of those plumps, the surface of the notum is globally smooth. In all specimens, many wide holes were observed on the surface of the dorsal notum ( Figs 45C , 46 ). Many small holes (diameter <10 µm) and many tufts of cilia were also found on the dorsal notum, including the rhinophores and the gills. In preserved specimens, the margins of the rhinophoral and branchial sheaths are smooth, although the branchial pocket seems to be elevated ( Fig. 45B ). There are six ( CASIZ 069612, CASIZ 097595 #2), seven ( CASIZ 113658), or eight ( CASIZ 097595 #1) tripinnate branchial plumes arranged in a circle around the anus. The rhinophores have 13 ( CASIZ 069612), 15 ( CASIZ 097595 #1 and #2), or 16 ( CASIZ 113658) lamellae.

The stomach is intermediary between a narrow, median pouch, and a free, large pouch ( Fig. 47A, C ). A caecum is distinguishable on the left, posterior side of the stomach. The intestine is straight and dorsal. The labial cuticle is armed with a pair of lateral jaw plates, and an additional, ventral plate ( Fig. 48 ). The rodlets are perpendicular to the surface of the labial cuticle, and seem to be ‘vertical’. Rodlet tips are irregularly shaped, pointed or rounded, and curved. Some (but not all) rodlet tips bear a distinct, posterior, pointed spur, and appear to be T-shaped. In one specimen (CASIZ 097595 #2), the jaw plates were extremely thick, due to many usual layers of additional rodlets. The radula is elongated: its length equals at least three times its width. The radular sac can be seen by dorsal dissection. Radular formulae were ( Fig. 49 ): c. 45 × (17-0-13) in a 16 mm long specimen (CASIZ 113658), c. 55 × (18- 0-12) in a 12 mm long specimen (CASIZ 069612),> 25 × (18-0-12) in a 35 mm long specimen (CASIZ 097595 #1), 53 × (21-0-14) in a 27 mm long specimen (CASIZ 097595 #2). Part of the radula of one specimen was lost during its preparation (CASIZ 097595 #1): the small number of rows is artificial. All radulae are asymmetrical: the number of teeth is higher on the left side than on the right side. The rachidian teeth are absent and the rachidian space is narrow. The rows of lateral teeth are at an angle of 45 degrees with the rachidian axis. The size of the lateral teeth gradually increases towards the margins, except for the three or four innermost ones and the last two outermost ones, which are much smaller. The hook of all lateral teeth is grooved on its outer edge. On the left side, the upper lip of this groove is expanded and ‘wing-like’. All teeth are hamate, except for the outermost one that can be vestigial (e.g. CASIZ 113658, CASIZ 097595 #2). Teeth have no denticles. The dorsal spur of the outermost teeth can be: absent on both sides (CASIZ 097595 #1 and #2); present on the left side but absent on the right side (CASIZ 069612); ambiguous (CASIZ 113658). The base of the last outermost tooth (or the penultimate if the last one is vestigial) can bear a spur (CASIZ 113658) or not (CASIZ 097595 #2); in some cases, I could not see this feature or it was ambiguous (CASIZ 097595 #1, CASIZ 069612).

The circum-oesophageal nerve ring is short ( Fig. 47B, D ). The cerebral and pleural are fused. They are fused with the pedal ganglia, or loosely separated from it. The surface of the ganglia is smooth.

The reproductive system is located on the right side of the body, between the buccal mass and the digestive gland ( Figs 47A , 50 , 51 ). The white ampulla is convoluted, with one or two loose loops. The division between male and female ducts (hidden within the female gland mass) could not be seen by dissection. The flattened prostate is divided in a proximal, whitish part, and a yellowish, distal part ( CASIZ 097595 #1 and #2). The prostate can also be homogeneously yellowish ( CASIZ 069612) or homogeneously whitish ( CASIZ 113658), probably because of non-natural factors. The white deferent duct is convoluted with several loose ( CASIZ 069612, CASIZ 113658) or tight ( CASIZ 097595 #1 and #2) loops. I have commonly observed this kind of variation in discodorid species. There is no distinct, permanent penis at the distal end of the deferent duct. The vaginal duct is straight. The fertilization duct is short, although it can present one loop ( CASIZ 097595 #2). The duct of the receptaculum seminis is short and straight. The deferent duct and the vaginal duct join and form a vestibule that may remain externally independent from the female duct. The disappearance of the fertilization duct into the female gland mass (where it connects to the fertilization chamber) is well marked by a short duct (it can only be seen when the receptaculum seminis is moved). The size of the bursa copulatrix equals two or three times the size of the receptaculum seminis. Both pouches are spherical-ovate and close to each other; the bursa copulatrix is partly covered by the prostate. The surface of both spermatic pouches is smooth. In the distal part of the reproductive system, there are several accessory glands that may be ramified and several stylet sacs ( Figs 50C–E , 51B–D ): two glands and two stylet sacs ( CASIZ 097595 #1); one gland and two stylet sacs ( CASIZ 097595 #2); three or four glands and two stylet sacs ( CASIZ 113658, CASIZ 069612). The glands are inconspicuous and their number is uncertain.

Diagnostic character: Phylidiella -like, dorsal pattern, acknowledging that it varies among individuals ( Figs 17D–H , 45A, B ).

Infra-specific character variation: Character variation was difficult to evaluate because I could only dissect four specimens and Bergh (1905) had incompletely described two specimens. However, a few features can be commented on.

The individual variation in the colour pattern fits within the kind of variation found in other discodorid species: the typical, diagnostic, black and white, dorsal pattern of liturata is phylidiella -like, but not all specimens have the exact same dorsal colour arrangement.

The number of radular rows ranges from 45 (CASIZ 113658) to 79 (holotype of liturata ); the number of teeth on the left side ranges from 18 to 21; and the number of teeth on the right side ranges from 12 to 14 (I do not consider the 20 teeth on the right side of the radula provided by Bergh in the original description).

As far as I can discern, the number of accessory glands and stylet sacs varies among individuals. However, this variation is jeopardized by the fact that these structures are not conspicuous and are very difficult to observe. In fact, I overlooked them when I first dissected these specimens ( Dayrat & Gosliner, 2005); Bergh also probably overlooked them for the original description.

Discussion: Bergh’s (1905) original description is largely incomplete. Most differences between the original description and the new description provided here are the result of the fact that Bergh probably overlooked some features (e.g. grooved oral tentacles, three jaw plates, etc.). Therefore, I do not see any incompatibility between Bergh’s original description of liturata and my observations.

However, the symmetrical, radular formula provided by Bergh remains a problem: it is unambiguously asymmetrical in all material dissected for the present study. My hypothesis is that Bergh overlooked this feature, because it really is exceptional: actually, it took me quite some time to ‘see’ it; it was Dave Berhens who first pointed out that a radula I was showing him ( CASIZ 099080; see sp. B) did not seem to be symmetrical; also, radular asymmetry is probably less obvious on a slide than on SEM pictures. Of course, it cannot be excluded that liturata could include specimens with both symmetrical and asymmetrical radulae (see erythraeensis ). Workers will have to dissect more individuals to determine whether the radula is always asymmetrical.

Bergh pointed out that the classification of liturata in Discodoris was uncertain, because of its external morphology and its jaw plates (probably the shape of the rodlets). Bergh, however, did not make a connection between the long, narrow radula of liturata and the long, narrow radula of four species he had described earlier – granulata , indecora , dubia , and egena . He probably did not think that it was necessary to compare liturata with other Discodoris species because, as he emphasized, its Phylidiella -like dorsal pattern was clearly distinct.

Finally, note that Marcus (1965) briefly mentioned the existence of liturata when he described D. lora , because both species have an elongated, narrow radula.

Figures

Figure 17. Live animals (except for D). A, Paradoris erythraeensis, CASIZ 157029, total length (preserved) = 20 mm. B, P. erythraeensis, SAM A32370, total length (preserved) = 17 mm. C, P. erythraeensis, CASIZ 099390, total length (preserved) = 14 mm. D, P. liturata, dorsal view of the holotype, after Bergh (1905: plate XIV, fig. 15), total length (preserved) = 14 mm. E, P. liturata, CASIZ 097595 (probably #2), total length (preserved) = 27 (#2) mm. F, P. liturata, CASIZ 069612, total length (preserved) = 12 mm. G, P. liturata, CASIZ 113658, total length (preserved) = 16 mm. H, P. liturata, picture from CASIZ slide collection (specimen not found). Colour pictures by T.M. Gosliner.

Figure 45. Paradoris liturata. A, anterior, dorsal view, CASIZ 097595 #1, scale = 5 mm. B, right, lateral view, CASIZ 113658, scale = 3.75 mm. C, mantle holes, CASIZ 113658, scale = 0.75 mm. D, ventral, anterior view, CASIZ 097595 #1, scale = 4 mm.

Figure 46. Paradoris liturata, dorsal notum. A, CASIZ 097595 #1, scale = 200 µm. B, CASIZ 097595 #1, scale = 20 µm.

Figure 47. Paradoris liturata. A, general anatomy, dorsal view, CASIZ 097595 #1, scale = 7.5 mm. B, buccal mass, nervous system and oesophagus, dorsal view, CASIZ 097595 #1, scale = 3 mm. C, part of the digestive system, CASIZ 113658, scale = 2.5 mm. D, central nervous system, dorsal view, CASIZ 113658, scale = 3.75 mm.

Figure 48. Paradoris liturata, jaw rodlets. A, CASIZ 113658, scale = 30 µm. B, CASIZ 113658, scale = 10 µm. C, CASIZ 113658, scale = 10 µm. D, CASIZ 069612, scale = 30 µm. E, CASIZ 097595 #1 scale = 20 µm. F, CASIZ 097595 #2 scale = 30 µm. G, CASIZ 097595 #2 scale = 10 µm.

Figure 49. Paradoris liturata, radular teeth. A, radula, CASIZ 069612, scale = 100 µm. B, rows, CASIZ 069612, scale = 100 µm. C, left rows, CASIZ 069612, scale = 30 µm. D, right rows, CASIZ 069612, scale = 30 µm. E, left, outermost teeth, CASIZ 069612, scale = 30 µm. F, right, outermost teeth, CASIZ 069612, scale = 30 µm. G, left, outermost teeth, CASIZ 097595 #2, scale = 10 µm. H, right, outermost teeth, CASIZ 097595 #2 scale = 20 µm.

Figure 50. Paradoris liturata, reproductive system. A, general view, CASIZ 097595 #1, scale = 1.6 mm. B, spermatic pouches and ducts, CASIZ 097595 #1, scale = 0.9 mm. C, distal part with two accessory glands and two stylet sacs, CASIZ 097595 #1, scale = 0.6 mm. D, distal part with one accessory gland and two stylet sacs (only one sac visible on this side), CASIZ 097595 #2, scale = 0.6 mm. E, distal part with one accessory gland and two stylet sacs, CASIZ 097595 #2, scale = 0.6 mm.

Figure 51. Paradoris liturata, reproductive system. A, general view, with three or four accessory glands and two stylet sacs in the distal part (only one sac visible on this side), CASIZ 113658, scale = 0.9 mm. B, distal part with three or four accessory glands and two stylet sacs (only one sac visible on this side), CASIZ 113658, scale = 0.75 mm. C, distal part with three or four accessory glands and two stylet sacs in the distal part (only one sac visible on this side), CASIZ 069612, scale = 0.5 mm. D, distal part with three or four accessory glands and two stylet sacs in the distal part (only one sac visible on this side), CASIZ 069612, scale = 0.5 mm.