Hypselodoris infucata (RuÈppell and Leuckart, 1830)

Johnson Aângel Valdeâs, Rebecca F., 2001, complex (Mollusca, Nudibranchia, Chromodorididae), with remarks the genus Brachychlanis Ehrenberg, 1831, Journal of Natural History 35 (9), pp. 1371-1398 : 1374-1386

Hypselodoris infucata (RuÈppell and Leuckart, 1830)

(®gures 1A, B, 2±9)

Doris infucata RuÈppell and Leuckart, 1828 ±30 [1830]: 34, pl. 10, ®gure 3.

Brachychlanis pantherina Ehrenberg, 1831 .

Doris diardii Kelaart, 1859: 267 .

Chromodoris crossei (Angas) : Bergh, 1905: 146 ±147, pl. 4, ®gure 6, pl. 16, ®gures 7, 8.

Chromodoris runcinata Bergh, 1877a: 479 ±482, pl. 51, ®gures 32, 33, pl. 53, ®gures 5±12; Eliot, 1904: 393 ±394; 1905a: 232±233; Barnard, 1927: 184; VayssieÁre, 1912: 46, pl. 1, ®gures 8a, b.

Chromodoris semperi Bergh, 1877a: 482 ±484, pl. 52, ®gues 1, 2, pl. 53, ®gures 13, 14, pl. 55, ®gures 2±7; Bergh, 1905: 147 ±148, pl. 4, ®gure 5, pl. 16, ®gures 9, 10; Eliot, 1905b: 246 ±247.

Chromodoris semperi Bergh , var. nigrostriata Eliot, 1905b: 247 ±248.

Chromodoris semperi Bergh , var. tenuilinearis Farran : Eliot, 1905b: 248.

Chromodoris diardii (Kelaart) : Eliot, 1908: 106 ±107.

Glossodoris diardii (Kelaart) : Risbec, 1953: 66.

Chromodoris iris (Collingwood) : Risbec, 1928: 139 ±141, ®gure 36, pl. 6, ®gure 1.

Glossodoris runcinata (Bergh) : O’ Donoghue, 1929: 726; White, 1951: 244 ±245, ®gure 8; Engel and van Eeken, 1962: 24.

Hypselodoris infucata (RuÈppell and Leuckart) : Narayanan, 1969: 198. Edmunds, 1971: 375 ±379, ®gure 17, pl. 1B; Thompson, 1972: 395 ±398 (in part), ®gure 1A, pl. 3, ®gures I±K; Rudman, 1973: 190 ±191, ®gure 7C, D; 1977: 386±387; Mienis and Gat, 1981: 51 ±52; Bertsch and S. Johnson, 1981: 62±63; S. Johnson and Boucher, 1983: 271; Gosliner, 1987: 81, ®gure 127; Burn, 1989: 763; Yonow, 1989: 302, ®gure 20; Debelius, 1998: 236; Gosliner and R. Johnson, 1999: 38±40, ®gures 13G, 24.

Hypselodoris obscura (Stimpson) : Willan and Coleman, 1984: 22, ®gure 55; Coleman, 1989: 35; Wells and Bryce, 1993: 114, ®gure 140; Debelius, 1998: 239.

Type material

HOLOTYPE of Brachychlanis pantherina : Suez, Egypt, Red Sea, 7.5 mm long, dissected, leg. Ehrenberg ( MHUB 607 ).

SYNTYPES of Hypselodoris infucata: El TuÃr , Egypt, Red Sea, seven specimens, 11±16 mm long, leg. E. RuÈppell ( SMF 219200 ) .

Additional material

Suez, Red Sea, 16 May 1914, one specimen, 14 mm long, leg. E. Bannwarth ( SMF 1145 ) .

As Sawda Island , Khalij al Halaaniyaat , Arabian Sea, Oman, October ± November 1993, one specimen, 12 mm long, leg. J. L. Earle ( CASIZ 097423 ) .

Coconut Island Marine Lab, Kaneohe Bay, Oahu , Hawaii, 10 February 1986, one specimen, 12 mm long, leg. M. T . Ghiselin and T . M. Gosliner ( CASIZ 061471 ); 12 February 1986, four specimens, 16±32 mm long, leg. M. T . Ghiselin and T . M. Gosliner ( CASIZ 087067 ); 25 October 1986, one specimen, 21 mm long, leg. T . M. Gosliner ( CASIZ 073107 ) .

Talumben , Bali, Indonesia, January 1998, two specimens, 17±20 mm long, leg. Mike Miller ( CASIZ 115231 ) .

Ligpo Island , Batangas Province, Luzon Island, Philippines, 0±12 m depth, 3 March 1995, two specimens, 10±12 mm long, leg. T . M. Gosliner ( CASIZ 105683 ) .

Hamilo Bay , Batangas Province, Luzon Island, Philippines, 1 m depth, 3 March 1995, two specimens, 24±27 mm long, leg. D. Behrens ( CASIZ 105690 ) .

Horseshoe CliOEs, WNW of Onna Village, Okinawa, Ryuku Islands, Japan, 6 m depth, 9 May 1987, one specimen, 21 mm long, leg. R . F. Bolland ( CASIZ 070231 ) .

East side of Bermier Island, Cleft Rock , Shark Bay , Western Australia, 5 m depth, 21 May 1995, one specimen, 17 mm long, leg. C. Bryce ( WAM 568-91 ) .

Distribution

This species is distributed throughou t the Indo-Paci®c, from the Red Sea ( Yonow, 1989) to Hawaii (Bertsch and S. Johnson, 1981). It has also been reported from the eastern Mediterranean ( Mienis and Gat, 1981).

External morphology

The living animals are up to 50 mm in length. The body is elongate and relatively high in pro®le, clearly higher in the middle region, where the posterior end of the foot emerges (®gure 1A, B). The general body colour is blue or greenish blue. There may be darker and lighter areas irregularly distributed on the dorsum. In some specimens the blue colour fades to paler blue in the middle of the dorsum. Dark blue and yellow spots (occasionally orange) are scattered over the entire dorsum. The yellow spots are larger than the dark blue ones and may be rounded, oval or occasionally very elongate. The posterior end of the foot is long, extending far beyond the mantle.

The perfoliate rhinophores are composed of 12±14 lamellae. They are white to bluish, with red or reddish orange lamellae. Occasionally the whole rhinophore is red. The gill is composed of 10 unipinnate branchial leaves, which are white with a red rachis on either both sides or only the outer side. Sometimes the most distal lamellae are all red and occasionally all of the lamellae are completely red.

Anywhere from three to 12 mantle glands are found on either side of the head (®gure 2A±G). Usually, the number of glands on either side is symmetrical. There are 10±26 mantle glands along the posterior edge of the mantle. Although the number of glands is variable, their position and distribution is not. The distribution patterns of mantle glands has been shown to be important in distinguishing between closely related species of Hypselodoris (Gosliner and R. Johnson, 1999) .

Anatomy

The buccal mass is divided evenly into an anterior glandular portion and a posterior muscular one. The jaws are composed of a number of elongate, unicuspid rodlets between 15 and 20 m m in length (®gures 3D, 4D, 5D, 6D). The radular formula for a 12 mm long Hawaiian specimen ( CASIZ 061471) is 39 Ö 41.0 .41. The formulae for specimens 17 and 20 mm long from Western Australia and Bali ( WAM 568-91; CASIZ 115231) range from 52 Ö 73.0 .73 to 63 Ö 97.0 .97, respectively. Rachidian teeth are absent. The innermost lateral teeth have two large cusps, with one shorter denticle on the inner side of the cusp (®gures 3A, 4A, 5A, 6A). The length of the inner denticle is extremely variable. The remaining lateral teeth are hook-shaped, have two cusps and lack denticles on both sides (®gures 3B, 4B, 5B, 6B). Some of the middle laterals of some specimens may have a minute, pointed denticle below the second cusp. The presence of these denticles is not consistent on one radula, much less in radulae from one locality. The outer laterals are short, having one to ®ve denticles situated under the second cusp (®gures 3C, 4C, 5C, 6C).

The reproductive system has a short, oval ampulla that divides into the oviduct and the prostate (®gure 7). The oviduct is short and enters the female glands near the centre of the mass. The prostate is long, tightly coiled with several loops. It narrows and then expands into a long, muscular vas deferens. The ejaculatory portion of the vas deferens is very short. The vas deferens is short and coiled, and opens into a common atrium with the vagina. The penis is unarmed. Near the exit of the female glands there is a large, rami®ed vestibular gland. The vagina is long and wide. The size and position of the seminal receptacle varies. In some specimens it emerges from the middle of the vaginal duct and is small and oval (®gure 7A, C, D), and in other specimens it is minute and emerges from the base of the bursa copulatrix (®gure 7B). The very long and convoluted uterine duct connects to the vaginal duct distally to the seminal receptacle connection.

Remarks

Thompson (1972) ®rst suggested that H. obscura and H. infucata were synonyms. He went on to note that the newly united species, H. infucata , was one of the most variable and widespread chromodorids. Even though he found slight radular variation between specimens from New South Wales, Australia and the east coast of Africa, he also detected signi®cant variation within diOEerent specimens from eastern Australia. He thought that the range of variability in Australian specimens was only slightly less than the range of variability between the Australian and East African specimens. He also detected similar variation in the colour patterns of these animals. We found slight radular variation in the specimens we examined, but none of our specimens lacks inner denticles on the innermost lateral teeth, as found by Thompson (1972) in a specimen from Queensland. Some of the specimens we examined have greatly reduced inner denticles that may be di cult to see using only a light microscope, as Thompson did, but they all have inner denticles. The only radular diOEerence found in this study is the presence of small, randomly placed denticles on the middle laterals of some specimens of H. infucata .

Rudman (1973, 1977, 1984) separated H. infucata and H. obscura into distinct species. He based his separation on the bicuspid inner lateral tooth found in some New South Wales specimens by Thompson (1972), the distinct colour pattern found in these same Australian specimens and the assertion that animals with this colour pattern were found only in eastern Australia. As mentioned above, all specimens we examined have an inner denticle on the innermost lateral teeth. In the ®gure used by Rudman to show the simply bi®d innermost laterals of H. obscura , there are small single inner denticles visible on the inner sides of the innermost teeth ( Rudman, 1984, ®gure 49A).

Gosliner and R. Johnson (1999) also retained H. infucata and H. obscura as distinct species. They thought these two species should remain separate due to diOEerences in coloration, the diOEerence in size of the muscular portion of the buccal mass in relation to the oral tube, diOEerences in the shape of the jaw elements, the apparent diOEerence in the lengths of the vaginal ducts, and the presence of lateral mantle glands in specimens of H. obscura . They did not examine any specimens of H. obscura , but rather relied on information from the literature ( Edmunds, 1971; Rudman, 1984). After examination of material from eastern Australia, many of the diOEerences used by Gosliner and R. Johnson (1999) cannot be found. The apparent, slight diOEerence in the proportion of the muscular buccal mass to the oral tube could be due to preservation, and could not be found in any of the specimens examined here. Jaw element shape can vary depending on where the rodlets examined are located on the jaw ( Ortea et al., 1996). Using the shape of jaw rodlets to separate species is questionable, unless the same portions of the jaw are compared in all cases. Based on drawings from the literature, Gosliner and R. Johnson (1999) stated that the vaginal duct length of H. obscura was shorter than the vaginal duct length in H. infucata . Vaginal duct length varied slightly in specimens examined here, but the variation was not consistent. The position and size of the receptaculum seminis varied more than any character we examined, except perhaps colour. In one specimen of H. infucata the receptaculum is very small and positioned just at the base of the bursa copulatrix (®gure 7B). In all other specimens examined the receptaculum emerges from the middle of the vaginal duct and is small and oval shaped, but there is even some variation in the placement and size in these specimens (®gure 7A, 7C, D).

The only consistent diOEerence we found between H. infucata and H. obscura is in the length of the ejaculatory portion of the vas deferens. All specimens examined from south-east Australia, the type locality of H. obscura , have a very long and convoluted ejaculatory portion of the vas deferens, whereas specimens from other Indo-Paci®c localities have a very short one. This is also consistent with the specimens studied by Rudman (1984), who clearly illustrated a very long and coiled ejaculatory portion of the vas deferens in H. obscura ( Rudman, 1984, ®gure 50). This long, coiled ejaculatory portion of the vas deferens is not present in any specimens of H. infucata examined. Even the specimen of H. infucata from Bali, which resembles H. obscura and has the same minute receptaculum seminis at the base of the bursa copulatrix, has a short ejaculatory portion of the vas deferens. It is not clear whether H. obscura is a diOEerent species from H. infucata , but since there is at least one consistent diOEerence we will provisionally maintain H. obscura as a separate species.

Specimens from Indo-Paci®c localities, other than south-east Australia, show a large degree of morphological and anatomical variation, and the anatomical diOEerences are not correlated with the geographic range nor with the external appearance of the specimens. Therefore, all specimens studied here, except for those from southeast Australia, are assigned to H. infucata . The references by Willan and Coleman (1984) and Coleman (1989) from Queensland are provisionally assigned to H. infucata in the absence of anatomical information.

Description of the holotype of Brachychlanis pantherina

The preserved specimen ( MHUB 607) is 7.5 mm long, 4 mm wide and 4 mm high, and it is in a very bad state of preservation. The shape of the body is oval. The mantle is slightly raised and wider in the centre of the body (®gure 8). The skin is extremely hard making dissection impossible, other than removal of the radula and jaws. The specimen has lost its original coloration, it is now uniformly dark brown, with a yellowish mantle margin. The dorsum is smooth, lacking tubercles, but the skin is folded forming a pattern of irregular, low ridges. In the areas surrounded by these ridges there are whitish deposits, probably formed as a consequence of the putrefaction or desiccation of the ¯esh. The mantle margin is narrow and folded. Mantle glands are not visible but ®ve empty holes, probably formerly occupied by mantle glands, are visible in the posterior end of the body. The anterior end of the specimen appears to be partially dissected from the ventral surface, but the radula and jaws were intact. The internal organs examined are very damaged and we were unable to recognize the diOEerent structures. Other external features such as the rhinophores or the gill are not visible. The placement of the gill can be inferred by a protuberance near the posterior end of the body.

The buccal bulb and oral tube were damaged so their morphology and relative size could not be observed. The jaw rodlets are elongate and quadrangular, with well-developed lateral ¯anges (®gure 9D). The rodlets from the central region connecting both jaws are smaller and irregular in shape. The radula is very fragile and the teeth are damaged. The radular formula is 25 Ö 26.0 .26. The inner lateral teeth have a prominent denticle on the inside of the bi®d cusps (®gure 9A). All the middle lateral and outermost teeth have bi®d cusps, and are devoid of denticles (®gure 9B). Some of the teeth appear to be deformed and partially dissolved, sometimes lacking the lower cusps (®gure 9C).

Remarks on Brachychlanis pantherina

Ehrenberg (1831) reproduced his ®eld notes on the living specimen of Brachychlanis pantherina describing the shape and colour of the animal:`Forma elongata bipollicaris, pollicem lata , dorso subtilissime papillosa, e X avicante cinerea maculis obscure fuscis variegata , duabus maioribus triangularibus inter tentacula ’ [Form (5animal) two thumbs (5inches) long (about 50 mm), one thumb wide (about 25 mm), with the dorsum very minutely tuberculate, and grey of various tones tending to dark yellow with black spots, with two larger triangular spots between the tentacles (5rhinophores)].`Pes dorso latior, utrinque rotundatus, X avicante albidus, rufo subtiliter adspersus, maculis subtus maioribus ’ [Foot wider than dorsum, rounded in both ends, white tending to yellow, with a minute sprinkling of reddish, with larger spots ventrally].`Proboscis terminalis albida cylindrica truncata brevis ’ [Proboscis terminal, cylindrical, short, cut oOE, whitish].`Tentacula duo dorsualia frontalia fuscescentia tetragona pyramidata, transverse sulcata, apiculo albido laevi terminata, in pallii incisura duplici frontali posita ’ [Two anterior-dorsal, brownish, tetragonal-pyramida l tentacles (5rhinophores), transversall y furrowed, ®nishing in a small white point, placed in two frontal holes of the mantle].`Tentacula duo labiala W liformia subulata albida ’ [Two labial tentacles (5oral tentacles), ®liform, perforated, whitish].`Branchiarum fasciculus unicus quinquelobus, in pallio ad margem posticum positus et in huius apertura integra recondentus ’ [A single bundle of gills with ®ve lobes, placed in the posterior mantle margin and completely hidden in its aperture].`Branchiarum laciniae bipinnatae, radiis hyalinis, pinnulis niveis ’ [Branchial leaves bipinnate, radius hyaline, pinnae whitish]. Àpertura analis tubiformis ex media branchiaru m basi emergens ’ [Anal opening tubular, emerging in the centre of the gills].

From this description it appears that the animal was already dead when it was studied. Ehrenberg (1831) always indicated when the animals were described alive, but in the case of B. pantherina he only commented that the animal was damaged due to putrefaction (`Animal admodum singulare putredine correptum periit ’). He did not say whether the animal was damaged before or after it was described, but several comments in the text, such as the gill was retracted into the cavity and the cylindrical shape of the proboscis, indicate that the animal was probably already dead. Nudibranchs killed by anoxia very often have the mouth area dilated in a cylindrical proboscis. The present condition of the specimen leads us to believe that it was damaged or dried and then preserved in alcohol. We have examined other specimens studied by Ehrenberg, such as the types of Hexabranchus praetextus Ehrenberg, 1831 , Asteronotus hemprichii Ehrenberg, 1831 and Actinocyclus verrucosus Ehrenberg, 1831 , which are in a perfect state of preservation.

There are several contradictions between Ehrenberg’ s (1831) original description and the present state of the holotype. The most outstanding is the diOEerence in size. When originally described, the specimen was about 50 mm long, now it is 7.5 mm long. However, cellular damage, due to dehydration could have caused a large reduction in size when it was preserved in alcohol. Bergh (1877b) found a length of 11 mm for the same animal, so it had also lost considerable length during the last century. Ehrenberg (1831) described the shape and colour of the rhinophores, but these organs are no longer visible in the holotype. He also indicated that the foot was larger than the dorsum, whereas now they are the same size.

Ehrenberg’ s (1831) description of B. pantherina agrees with the external appearance of Hypselodoris infucata RuÈppell and Leuckart, 1830 , re-described by Rudman (1977) and Gosliner and R. Johnson (1999), except for a few details. The size and body colour of B. pantherina ®ts within the range of H. infucata . Ehrenberg (1831) described the rhinophores of B. pantherina as being brown with white apex. This description is consistent with the colour pattern of the rhinophores of H. infucata , except that in living animals of this latter species they are red. However, it is very likely that in Ehrenberg’s dead specimen the red colour had changed to brown. We have examined several preserved specimens of H. infucata ( CASIZ 070231, CASIZ 105690) which have uniformly pale brown rhinophores with a lighter apex. The gill colour of B. pantherina was described as white, probably because it was hidden in its cavity with only a portion showing. In the light of present knowledge of the chromodorid fauna of the Indo-West Paci®c, there are no other species that ®t with the colour described for B. pantherina . According to Gosliner and R. Johnson (1999), the innermost lateral teeth of H. infucata have a prominent denticle while the middle lateral teeth very often lack denticles (®gures 3A, 4A, 5A, 6A). This is identical to the radula of the holotype of B. pantherina . However, Gosliner and R. Johnson (1999) found two to three small denticles in the outer lateral teeth of H. infucata that are absent in B. pantherina . In this latter species the outermost lateral teeth appear to be partially dissolved and in many cases they lack the lower cusp (®gure 9C). The jaw rodlets (®gure 9D) appear to be identical to those previously described for H. infucata .

In addition, the type locality of B. pantherina ®ts in the geographic range of H. infucata , which has been also reported from the Red Sea ( Yonow, 1989).

Although the original description of Brachychlanis pantherina is incomplete, the holotype is not well preserved and we were unable to study the reproductive system morphology, there is enough evidence that clearly indicates that this taxon is conspeci®c with H. infucata .

The synonymy of Brachychlanis pantherina and Hypselodoris infucata has no nomenclatural implications. According to Winckworth (1942), the speci®c name H. infucata was introduced in 1830, by RuÈppell and Leuckart along with other species of dorids. Therefore, it is a senior synonym of B. pantherina , which was introduced one year later. The older name H. infucata is much more widely used in literature than B. pantherina (only used once), so no changes in the present situation are needed.