Pellibranchus cinnabareus, a New Genus and Species of Non-Pelagic Nudibranch Mollusc of the Family Phyllirhoidae.
[Read before the Wellington Branoh, October 27, 1943; received by the Editor, November 18, 1943; issued seperately, June, 1944.]
Pellibranchus cinnabareus n.g., n.sp. is a small Nudibranch which up to the present time has been found only at Island Bay, Wellington, New Zealand. The limaciform adult, bright red in colour, lacks external gills and other appendages with the exception of a pair of relatively long tentacles on the head. The adults are found at all seasons of the year on the lower surface of stones in tidal runnels along the shore. The general form resembles that of a small lithophilus Elysiomorph but the uniform bright red colour extending over the sides and the foot, the possession of a multiseriate radula, and the division of the hermaphrodite gland into male and female acini enable the separation of this species from the known New Zealand Nudibranchs similar in size and habit. Packets of three to twenty-four eggs the same colour as the adults, are found from September to May. Development is direct, the animal hatching in the juvenile form. Graphic reconstruction after the technique of Wells (Proc. Zool. Soc., 1922, Part 4) was employed in determining much of the internal morphology.
The writer wishes to express her thanks to Professor H. B. Kirk for his valuable guidance and advice. The work has been conducted in the laboratory of the Biology Department, Victoria University College.
Pellibranchus cinnabareus belongs to the Sub-order Dendronotaceae (Odhner, 1936) including “holohepatic or cladohepatic Nudibranchs with the right liver smaller than, but similar in structure to the left. No blood gland. Only one vesicula seminalis. Rhinophores retractile into sheaths. Anus lateral or latero-dorsal in the interhepatic space.” It is referred to the family Phyllirhoidae (Odhner, 1936) since it possesses the “Back margin entirely reduced as well as the cerata. Anus lateral or dorsal. Liver consisting of two dorsal coeca (right and posterior liver) and one ventral (left anterior liver) all simple tubuliform. Rhinophore club smooth (in contraction falsely laminated); sheaths very small. Jaws covering the frontal side of the pharynx. Gonad in a few globular masses or floccular stripes. No prostata and no bursa copulatrix (but a muscular vesicula seminalis in the end of the oviduct). Nephroproct in the middle of the right side. Eyes with indistinct optic nerves.”
It should be noted here that Pellibranchus is benthic and not pelagic as are the other members of the family Phyllirhoidae and shows a remarkable convergence with the genus Cenia (Alder and Hancock) Sub-order Sacoglossa (Ascoglossa) in habitat and external form.
Pellibranchus differs from Cenia in having the hermaphrodite gland divided into male and female acini instead of spheroidal hermaphrodite lobules, genital orifices contiguous not distant, the anus in the second quarter of the body not posterior, and a multiseriate not uniserial radula. These features of Pellibranchus clearly place the genus within the Sub-order Dendronotaceae and establish the similarity in external form of Pellibranchus and Cenia as one of simple convergence.
Odhner (1936) defines two genera in the family Phyllirhoidae:
“Genus: 1. Phylliroe Péron and Lesueur.
Body elliptical without a foot. Anus lateral, dextral. Gonad in spheroidal globuli. Liver coeca four (two superior and two inferior ones). Head without a disc. Jaws with processus masticatorius. Radula well developed, with a few lateral teeth denticulate in the inner edge and a median tooth denticulate on both sides. Penis cylindrical, tube-like; its glans armed with conical papillae and with a large sub-apical lobe.
Genus: 2. Cephalopyge Hanel.
Body elongate, lanceolate, with a distinct foot. Anus dorsal close behind rhinophores. Gonads flocculent, in stripes or in clusters of folliculi. Liver cocea usually 3 (a single dorsal one, a single ventral as a rule, and a posterior). Head with a disc. Jaws without the processus masticatorius. Radula often obliterated. Penis conical and unarmed.”
The present species possesses a distinct proboscis; rhinophores linear, bluntly tipped and retractile, about a millimeter in length; hepatic caeca three, all bluntly lobed; rectum directed forwards; anus opening in the mid-dorsal line in the second quarter of the body; foot quite distinct and terminating in a tail; penis armed with hooked spines; accessory genital glands present; hermaphrodite gland divided into male and female acini, with distinct male and female ducts; penial and vaginal apertures surrounded by a conical copulatory pouch which can be extruded through the genital aperture on the right side of the body; jaws wanting but the buccal bulb armed internally and externally with a supporting connective tissue sheath, which forms a cone of sclerites round the true mouth; radula narrow, formula 18.104.22.168.1.; development direct.
These features are distinct from those of the existing genera in the family, and it is therefore proposed to erect a new genus with the following characters:—
Genus: 3. Pellibranchus nov.
Body limaciform with a distinct foot. Anus opening about the mid-dorsal line in the second quarter of the body. Gonads divided into male and female acini, the female lobes spherical, the male lobes more elongate. Liver caeca three (a left anterior dorsal liver, large posterior liver and right anterior liver poorly developed). Head without a disc. Jaws without processus masticatorius. Radula well developed. Penis armed with hooked spines.
Genotype: Pellibranchus cinnabareus n.sp. Wellington, N.Z.
P. cinnabareus is unique in the family Phyllirhoidae in the relation of the anus and nephroproct, the absence of functional jaws, the thick body wall with uniform ciliation, and in its non-pelagic habit. Within the family it resembles Phylliroe in having the nephroproct in association with the anus but is unlike that genus since these structures in P. cinnabareus are in the dorsal position whereas in Phylliroe the nephroproct is on the right side of the body. The association of the nephroproct and anus is general in the Dendronotaceae (Odhner, 1936), but in the members of the family Phyllirhoidae the nephroproct lies about the middle of the right side and lacks constant relationship with the anus. Accordingly too much significance may not be attached to this feature in the family.
Pellibranchus has no chitinous sclerites in the buccal bulb that could function as jaws in the usual meaning of the word, but covering the bulb internally and externally is a membranous connective tissue sheath, forming round the frontal portion of the true mouth a cone of sclerites usually twelve in number. The writer has not observed that these function as jaws. There is some variation in the shape of the jaws in other members of the family, Cephalopyge being without the usual processus masticatorius of Phylliroe. Odhner (1936) considers this the primitive condition.
Pellibranchus is more nearly allied to Cephalopyge than to Phylliroe both genera having a distinct foot and dorsal anus. In Cephalopyge there are usually three liver caeca, but the number and size is variable. In Pellibranchus the liver is more compact, with three well defined caeca in which the left anterior liver appears dorsal in position, not the right as is the case with the other members of the family. The right hepatic caecum in Pellibranchus is ventrolateral in position and generally obscured in lateral view by the anterior genital mass. (Plate 9.) Odhner (1936) discussing the difference in the liver structure of the closely allied genera Fimbria and Melibe considers that the differences “may be due to the various formation of the gonad which stands in intimate correlation to the liver.” Possibly the great development of the anterior genital mass in Pellibranchus can be correlated with the reduction of the right anterior liver. Slight divergence is seen in the fact that Pellibranchus has bluntly lobed caeca, while in Cephalopyge these structures are simple and tubular, although too much significance may not be attached to this distinction as Hoffman (1906) states that Vesschelli observed some variation in the liver of Phylliroe, where one specimen bore a few small diverticulae and in another they were totally atrophied.
Odhner (1936) further states that “the liver of nudibranchs shows a tendency to disintegrate from a compact to a more or less branched organ, and that the liver may consequently show the same stages of disintegration in different families, as well as different stages within the same family; therefore it is not apt as a direct indicator of relationship.”
The absence of a disc on the head of Pellibranchus further distinguishes it from Cephalopyge, and the distinct nature of the two
genera is established by the following structures of Pellibranchus: the penis is armed with hooked spines; no ampulla is developed on the hermaphrodite duct; an albumen gland is present as well as a mucous gland; separate male and female ducts leave the hermaphrodite gland. At the same time the known species of Pellibranchus superficially resembles C. trematoides, being very similar in size, shape and colour, but the number of gonads in P. cinnabareus is seven, two ventral sperm lobules, and five dorsal ovarian lobules, whereas in C. trematoides there are five hermaphrodite lobules.
Although the genus Pellibranchus is assigned to the family Phyllirhoidae it may be necessary ultimately to create a new family or amend the present family definition to include this genus on account of its unique features, but the writer at present is unwilling to do this in view of the general agreement with the existing genera.
Pellibranchus cinnabareus is a small, bright red marine slug, exhibiting external symmetry. The body is arched, limaciform, with the dorsal and lateral surfaces smooth. The colour is uniform over the body except the tips of the rhinophores and the tail, which are a paler vermilion. The body appears granular, and when the animal moves wave-like ridges pass over the entire surface of the animal. The visceral hump grades imperceptibly into the foot, which is simple and terminates in a small pointed tail into which the viscera do not extend. The liver shows through the lateral body wall as a dark green brown mass. The eyes appear as small black dots situated behind the tentacles and in a straight line with the tentacular base. The size of sexually mature animals ranges from 3 mm. to 6 mm. with an average length of 4 mm. and vertical central diameter of 1–5 mm.
The structure of the body wall and associated connective tissue has been described by several workers for the genera Cephalopyge and Boopis. In many respects Pellibranchus shows a body-wall structure different from that of these two genera, but glands similar in structure to those described for these two genera are found in Pellibranchus opening between the epidermal cells and are most numerous in the foot and tail region. In the present species the epithelium is ciliated and columnar over all parts of the body, and the body wall is heavy. This is not the case with the other two genera of the family where the epidermis is flattened and unciliated and the body wall on the whole much thinner. The prominent longitudinal muscle strands described by Stubbings (1937) for Cephalopyge and Dakin and Colfax (1936) for Ctilopis picteti (Cephalopyge orientalis) are not distinguishable in Pellibranchus. In the central dorsal aspect of the body of Pellibranchus, is a large branched multicellular slime gland opening to the exterior close to the anus. Hecht (1895) described an anal gland in the Nudibranch Proctonotus mucroniferus. In Proctonotus the gland opens into the intestine, but in Pellibranchus it opens directly to the exterior.
The alimentary canal (Plate 9) comprises in general a buccal bulb with the related structures of radula and odontophore, a long oesophagus, stomach, intestine and digestive gland or “liver”.
The buccal bulb is pear-shaped, enclosing the radula and odontophore with their accompanying muscular attachments. The odontophore “cartilages” usually present in molluses (Pelseneer, 1906) appear to be absent in Pellibranchus. In almost the same position as the cartilages in other molluses, and immediately under the sub-radula membrane is an infraradula sheet of longitudinal muscle fibres. These are inserted dorso-laterally on to the large circular muscle fibres of the odontophore. Inserted on to the ventro-lateral portion of the odontophore are longitudinal muscle fibres that have their origin in and are continuous with the ventro-lateral external longitudinal muscle fibres of the buccal bulb. The radula sheath lies embedded in the muscle fibres at the posterior end of the buccal bulb. The radula has quite a sharp ventral bend bringing it to the under side of the odontophore, where it passes round the end of its flexible muscular support. The radula and odontophore are capable of extrusion through the opening of the true mouth—i.e., the aperture of the buccal bulb, by the contraction of protractor muscle fibres—those inserted laterally on to the odontophore. The entire buccal bulb can be drawn forward through the puckered orifice on the ventral surface or back into the introvert by contraction of retractor muscle fibres passing from its walls to the body wall.
Pelseneer (1906) has distinguished several varieties of protrusible molluscan buccal bulbs. The proboscis of Pellibranchus is pleurecbolic since when evaginated the oesophagus forms its inner lining and when invaginated its posterior continuation. A relatively thick membranous connective tissue sheath covers the bulb internally and externally forming twelve plate-like projections round the true mouth. These do not function as jaws. There are relatively large vascular lacunae scattered between the muscle layers of the buccal bulb.
The radula (Plate 8, Fig. 2) is narrow and formed of distinct but colourless teeth. In the absence of a central tooth the thin sub-radula membrane is visible down the centre of the ribbon. There are three rows of teeth on either side of the sub-radula membrane, two rows of laterals and one row of marginals. The teeth of the first row of laterals are grooved and the side of each tooth distant from the sub-radula membrane tapers away under the second row of laterals. Each tooth has a small, forwardly directed spinous process which emerges from the middle of the anterior margin of the tooth. The next row of laterals consists of crescent-shaped teeth broadly rounded laterally and with a sharp, spinous process arising from the concave anterior surface just medial to the rounded portion. The radula formula is thus 22.214.171.124.1. In each of the six rows of teeth of a sexually mature animal there are 45 individual teeth, making a total of 270 teeth in all. The oesophagus enters the buccal cavity dorsally by a narrow duct. As the oesophagus emerges from the buccal bulb it narrows and flexes down toward the ventral surface. About the midpoint of the body the oesophagus again flexes dorsalwards and opens into the stomach. The stomach is a broad chamber. Ducts from the left and posterior liver enter the stomach dorsally and from the right liver laterally. The intestine is a narrow, thick walled ciliated duct
Fig. 1. Packet of Eggs.
Fig. 2. Portion of Radula.
Fig. 3. T.S. Kidney.
Fig. 4. Reconstruction of the Central Nervous System. (Dorsal view.)
Explanation of Lettering.
AG., albumen gland; AHC., anterior hepatic caecum; AU., auricle; BB., buccal bulb; C., pedal commissure; CG., cerebral ganglion; CF., copulatory funnel; CN., cerebral nerve; DTG., distal tentacular ganglion; DVS., duct from vesicula seminalis to oviduct; E., egg; F., foot; G., ganglion; GS., granules embedded in ground substance of kidney; IM., inner membrane of egg; INT., intestine; K., kidney; KD., kidney duct; L., lateral teeth of radula; LN., lens; M., marginal teeth of radula; MG., mucous gland; N., nucleus; OC., optic cup; OD., oviduct; OE., outer envelope surrounding all the eggs; OES., oesophagus; OL., ovarian lobule; PG., pedal ganglion; PHC., posterior hepatic caecum; PL.G., pleural ganglion; PL.N., pleural nerve; PN., pedal nerve; PTG., proximal tentacular ganglion; S., sclerites; SL., sperm lobule; SRM., sub-radula membrane; ST.G., stomatogastric ganglion; T., tentacle; TA., tail; TGS., thread-like ground substance of the kidney; TN., tentacular nerve; V., ventricle; VD., vas deferens; VE., vas efferens; VS., vesicula seminalis; W., wall of kidney.
running from the upper left surface of the stomach. It travels on the left side of the body as far forward as the kidney, then flexes to the right, passes above the oesophagus and opens to the exterior slightly lateral to the mid-dorsal line. Salivary glands were not identified.
The nervous system (Plate 8, Fig. 4 and Plate 9) consists of a circumoesophageal nerve ring of six large ganglia, cerebrals, pleurals, and pedals. The cerebrals, like those described by Dakin and Colfax (1936) for Ctilopis picteti (Cephalopyge orientalis) are in apposition. The pleurals about half the size of, and lying behind the cerebrals are not continuous but marked off from the latter by distinct furrows. The pedal ganglia are of approximately the same size as the cerebrals but set more to the lateral aspect of the oesophagus, bringing them into contact with the cerebrals and pleurals, but distant from each other, and it is difficult to trace the sub-oesophageal commissure connecting them. This condition is similar to that described by Dakin and Colfax (1936). The stomatogastric ganglia lying close together under the oesophagus are joined by commissures to each other and the cerebrals. Three nerves from the anterior, dorsal and lateral aspects of the cerebrals can be distinguished in P. cinnabareus. The dorsal nerve is ganglionated, and this corresponds closely to the conditions existing in Ctilopis picteti (Cephalopyge orientalis) where two of the nerves emerging from the cerebrals are ganglionated.
The eyes lying under the epidermis in close contact with the cerebral ganglia are similar in structure to the gastropod eye described by Pelseneer (1906) and innervated from the cerebrals by a very short nerve entering the base of the optic cup. In P. cinnabareus the otocysts touch both the cerebral ganglia and pedal ganglia, as is the general rule, but I have been unable to trace a nerve connection with either of these ganglia. The rhinophores differ in form from the other members of the family but in internal structure are similar, showing very well the numerous deeply staining round or ovoidal cells which Stubbings (1937) in Cephalopyge arabica considers as similar to the gland cells described by Pierantoni for other members of the family. The nervous system is similar in most respects to the other members of the family but differs from them in having the cerebral and pleural ganglia as distinct entities, instead of being fused to form cerebro-pleurals. Also the eyes of the present species are not “simple pigment spots” as in Cephalopyge arabica but have a definite optic cup and lens.
The excretory system (Plate 8, Fig. 3 and Plate 9) consists of a simple spherical kidney situated dorso-laterally in the middle of the body. A narrow ciliated duct runs from the dorsal surface of the kidney opening externally just in front of the anus. No trace of a renopericardial duct could be found. The spherical form of the kidney appears to be unusual. Pelseneer (1906) states that in the majority of molluscs the kidney is a compact lobed mass, and in a large number of Nudibranchs (Doridomorpha, Janus, etc.) the kidney is highly ramified. Histologically the kidney of P. cinnabareus has very much the appearance of a disintegrating gland. The outer wall of the kidney is thin with prominent nuclei. The main portion shows
granules embedded in a thread-like ground substance in which no cellular structure is visible. Hecht (1895) figures a cross section of the kidney of Doris tuberculata in which the walls are thrown into folds and the cavity filled with long cilia. If the cellular walls broke down in the kidney of Doris tuberculata a structure very similar in appearance to the kidney of P. cinnabareus would result. The disintegrating appearance of the kidney is probably of some importance in distinguishing the present genus when it is pointed out that in the anatomical sub-division of the family Phyllirhoidae given by Dakin and Colfax (1936) the classification is based on the presence or absence of a renal organ. This is the only attempt I have seen of a primary sub-division of the family on this basis. Cells in other regions of the body, namely certain cells of the “liver” and the numerous “Cells of Leydig” in the body wall probably perform the function of excretion as has been indicated by Hecht (1895) for Doris tuberculata and Eolis glauca and Yonge (1926) for several other Nudibranchs.
In the vascular system (Plate 9, Fig. 1) the heart is dorsal just beneath the connective tissue of the body wall and to the anterior end of the body. The ventricle is anterior to the auricle and separated from it by a muscular constriction. Ventricle and auricle are of almost equal size, and the pericardium is very poorly developed, consisting of only a thin layer of loose connective tissue. There are no respiratory organs in P. cinnabareus.
The reproductive system (Plate 9) is divided into two portions, the hermaphrodite gland and the anterior genital mass, the ovarian and sperm ducts being present as a bridge between the two. The hermaphrodite gland is elongate, composed of several contiguous acini bound together but separated by a limiting membrane. The lower portion is divided into two sperm lobules and the upper into five ovarian lobules, of which there are two on the right side and three on the left. This arrangement has been in general constant for the adult specimens examined. The ovarian lobules open into the lower sperm lobules. Opening from and running beneath each sperm lobule are delicate narrow vasa efferentia which unite at the anterior end of the foremost sperm lobule and enter the duct from the vesicula seminalis just before its junction with the upper ovarian duct. The vesicula seminalis is spherical, with thin muscular walls. The vas deferens leaving the vesicula coils back on itself in an “S” shaped bend and opens into the penis. The penis is oval and armed with hooked spines. The oviducal portion of the female organs consists of an albumen-mucous gland complex. The albumen gland lies mainly above and opens into the dorsal surface of the mucous gland. The mucous gland is sac-like and continuous with the vagina. The end of the vas deferens, penis and vagina are enclosed in a conical pouch covered with long cilia on the free edge and outer surface. There appears to be two kinds of motile sperm, some that are relatively large in size with pointed head and long tail twisted just below the head and others that are much smaller in size. Up to the present I have been unable to discover which kind of sperm fertilises the eggs. So far it has not been possible to distinguish the two kinds in the spermary.
The writer has not observed the oviposition of eggs (Plate 8, Fig. 1), but has found them at the eight celled stage and apparent blastula stage 21 days and 23 days respectively after copulation. The eggs are found in the same habitat as the adults. The number deposited varies from three to 24, with an average of 12 based on 50 packets. Investing the egg is a clear, thick membrane. Each egg membrane adhers to its neighbour where it touches, and enclosing all the eggs is a thinner clear capsule which is fastened to the surface of the rock. The eggs are spherical and have the same uniform vermilion colour as the adults. Eggs have been found in the natural habitat from September to May. Segmentation follows the usual spiral pattern, and development is direct, the animal hatching in the juvenile form. Pelseneer (1899 Trav. Stat. Zool. Wimereux, vol. vii) has described direct development in the Nudibranch Cenia cocksii, but this work is not available to the present writer and no comparison can be made.
Pellibranchus cinnabareus n.g. n.sp. is described and assigned to the Sub-order Dendronotaceae, Family Phyllirhoidae. The new genus is characterised by: a limaciform body with distinct foot. Anus opening about the mid-dorsal line in the second quarter of the body. Gonads divided into male and female acini, the female lobules spherical, the male more elongate. Liver caeca three (a left anterior dorsal liver, large posterior liver and right anterior liver poorly developed). Head without a disc. Jaws without processus masticatorius. Radula well developed. Penis armed with hooked spines.
Within the family Pellibranchus appears most closely allied to the genus Cephalopyge. Up to the present time specimens are known only from Island Bay, Wellington, New Zealand.
Dakin, W. J., and Colfax, A. N., 1936. Ctilopis, a Rare Pelagic Nudibranch of the Family Phyllirhoidae (Bergh). Proc. Zool. Soc., London, (11), pp. 455–460.
Hecht, Emile, 1895. Contribution a P'étude des Nudibranches. Mem. Soc. Zool. de France, tome. viii, pp. 539–711.
Hoffman, H., Opisthobranchia, in Bronn's Klassen u. Ordnungen des Tierreichs. Leipzig, 1932.
Odhner, Nils. Hj., 1936. The Dendronotaceae: a Revision of the System. Melanges de P. Pelseneer. Musée Royal D'Histoire Naturelle de Belgique. (Mem.) Deuxieme Serie. Fase. 3, pp. 1057–1128.
Pelseneer, P., 1906. Treatise on Zoology, vol. v. Edited by E. Ray Lankester.
Stubbings, H. G., 1937. Phyllirhoidae. John Murray Expedition, 1933–1934. Scientific Reports. (B.M.N.H.), vol. v. no. 1, pp. 1–14.
Yonge, C. M., 1926. The Digestive Diverticula in the Lamellibranchs. Trans Roy. Soc. Edin., vol. liv, Part 3, pp. 703–718.