Philine exigua n.sp. (Opisthobranchia: Bullomorpha), a Minute Interstitial Species from Melanesia

Transactions of the Royal Society of New Zealand : Biological Sciences, Volume 11, Issue 12, 15 October 1969, Page 177

Philine exigua n.sp. (Opisthobranchia: Bullomorpha), a Minute Interstitial Species from Melanesia

D. A. Challis

By

Department of Zoology, University of Auckland

[Received by the Editor, 3 April, 1969.]

Abstract

A new species of Philine collected from intertidal shell-sand, Guadalcanal, British Solomon Islands Protectorate and from Efate in the New Hebrides is described with an account of its internal anatomy. It is suggested that this is an interstitial species.

Introduction

Several minute interstitial opisthobranchs have recently been described from the marine sands of the Melanesian area (Challis 1968, 1969 a). These animals were collected during the interstitial fauna survey carried out by the 1965 Royal Society expedition to the Solomon Islands Protectorate. Challis (1969 b), has given a general ecological account of these animals, their distribution, and a description of the beaches in which they live.

Materials and Methods

A detailed account of the methods used in collecting, isolating, photographing and preserving the opisthobranchs has been given in the above account. Preparations of the radula and gizzard plates were made by dissolving away the soft parts of the animal in 10 per cent potassium hydroxide and mounting the hard parts in Salmon's (1949) polyvinyl-lactophenol with Chlorazol Black. Specimens were sectioned in transverse, longitudinal and horizontal planes and reconstructions of the anatomy were prepared. Where the details of the anatomy were complicated, as in the reproductive system, the sections were each drawn with the aid of a camera lucida and large scale stereographic diagrams were made. The central nervous system was dissected.

All drawings other than reconstructions were made from photographs or with the aid of a camera lucida.

Family PHILINIDAE Genus Philine Ascanius 1772

Philine exigua n.sp.

Description: Fully extended, sexually mature animal (Fig. lc and Id) approximately 2.5 mm long, ratio of length to breadth approximately 1:4, ratio of length of head shield to visceral hump approximately 1:2.5, parapodia reduced to a very slight lateral extension of the foot noticeable only in preserved specimens. Visceral hump, separated anteriorly from the head shield by a deep transverse groove; extending posteriorly beyond the foot for approximately a third of its length; terminating in a pair of overlapping tail processes (Fig. la) forming the

posterior wall of the mantle cavity. Notum and foot separated by a deep longitudinal groove partially enclosed by the lower edge of the notum and the reduced parapodial part of the foot. Notum and foot epithelium completely ciliated, longitudinal groove not generally ciliated but having several narrow longitudinal tracts of long cilia on each side. Shell internal, small, situated beneath the surface of the posterior third of the visceral hump. Because the animals were fixed in Bouin's fluid for about 12 hours the shells of the specimens were completely destroyed, only the shell membrane remaining. Gill lacking. Colour in life opaque white with a large yellowish or orange spot indistinctly visible through the epidermis of the visceral hump. Two eyes present, but not visible externally. Radular formula 1-0-1 X 19 (Fig. le). Tooth base (Fig. If and lg) broad, flat, with flanged muscle attachment processes near the posterior edge, distal portion of the tooth tapering and bending inwards and slightly posteriorly at right angles to the plane of the flattened base, with a shallow denticulate ridge running parallel to the anterior edge of the distal portion. Three calcareous gizzard plates (Fig. 2b), one situated dorsally and two ventrolaterally within the gizzard. Dorsal plate roughly lozenge-shaped, widest in the middle region and drawn out and rounded at each end, ventrolateral plates much larger and in the form of shallow elongate isosceles triangles with rounded ends. All plates roughly triangular in cross section (Fig. 2d).

Type Locality: The holotype was collected by the author in mid-August, 1965, from coarse, clean shell-sand at Low Water Neaps 500 yards southwest of the Agricultural Advisory Station, Komimbo Bay, West Guadalcanal.

Other Localities: Specimens were collected at a number of other stations at Komimbo Bay and from the same tidal level at Pango beach, Efate, New Hebrides. The precise locality of the Komimbo Bay stations together with the numbers of P. exigua collected at each is given by Challis (1969 b).

Types: A total of 64 specimens of P. exigua was collected. Of these 16 remain the others having been dissected or sectioned. The holotype together with nine paratypes and a slide of the radula and gizzard plates of a further paratype has been deposited in the British Museum (Nat. Hist.). A series of five paratypes together with a slide of the radula and gizzard plates of a further paratype has been deposited in the Dominion Museum, Wellington, New Zealand. The remaining paratype will be retained by the author together with the sectioned material.

Remarks and Biology

While the division of the body into head shield and visceral hump, the possession of three gizzard plates, the radular type and the presence of an internal shell place P. exigua within the genus Philine the animal differs markedly in a number of respects from the previously described species. The ratio of the length of the head shield to that of the visceral hump and of length to breadth together with the reduction of the lateral parapodia give P. exigua an unusually elongate and streamlined body form while the dissimilar shape of the gizzard plates, the arrangement of the reproductive system, the lack of a gill and the possession of a " pallial gland " further differentiate it from the existing species.

The present species was collected from coarse, clean, highly oxygenated sand in the vicinity of low water neaps. The animal was first found at Komimbo Bay, West Guadalcanal where it occurred in some numbers in company with several other interstitial opisthobranchs. Although the other opisthobranchs were later collected from a number of localities P. exigua was, surprisingly, not taken again within the Solomon Islands, but was later collected in small numbers from Pango beach near Port Vila in the New Hebrides group.

While a number of very small species of Philine have previously been described, P. cingulata Sars 1878, 2mm; P. denticulata Adams 1800, 2.5 mm, they have been dredged specimens and little has been recorded about their habitat. It has not previously been suggested that these animals are interstitial molluscs in the same sense as are the Acochlidiacea and the Philinoglossacea. The smaller Philinidae seem to have generally been thought of as animals burrowing through the sand in

the manner of their larger relatives rather than as animals moving like the Acochlidiacea, with a minimum of disturbance through the interstices of the sediments in which they live. The sand samples containing the animals were taken by simply scooping off the top two inches of sand and without the use of a core sampler with which the original stratification of the sand would be retained it is not possible to say with certainty that P. exigua is an interstitial animal. A comparison of the animal's size with the particle size of the sediment from which it was collected indicates this mode of existence. It is unlikely that an animal of the dimensions of the present species could successfully burrow in the sediment in which it was found for more than 60 per cent of the particles were between .5 and Imm in size. Furthermore, the larger Philinidae although they are both relatively powerful animals by comparison with the present species and highly adapted for sand burrowing are usually recovered from sand of a fine and more even texture.

An interstitial habitat is also indicated by the unusual body proportions of the animal. The exceptional elongation of the head shield, the reduction of the visceral hump and the lateral parapodia give the animal a shape that is eminently suited to life in this environment. This elongation, though not as extreme as in the Pseudovermidae, for example, appears to be an instance of the general tendency to vermiformity exhibited by many interstitial members of other families, a tendency commented on by Swedmark (1964) and others.

The Anatomy of Philine exigua

Alimentary Canal (Fig. 2a) : Mouth situated in the anterior transverse region of the lateral groove (Fig. lb). In material stained in Mallory/Heidenhain it is surrounded above and below with strongly cyanophilous oral glands discharging into the lumen immediately inside the external opening (Fig. 4c). Mouth j connected to the buccal cavity by a thin-walled oral tube. Buccal cavity more complex histologically than the oral tube and showing four well-differentiated tissue layers; an epithelial layer internally, an inner circular and longitudinal muscle layer, an outer circular muscle layer and, between the two latter, a considerable space filled with a network of radial muscle fibres, like those described by Brown (1934) from Philine aperta (Linne). Radula sac opening into the ventral surface of the buccal cavity, radula supported on a very muscular odontophore (Fig. 2c). Salivary glands paired, discharging into the posterior end of the buccal cavity very near the junction of the crop and the buccal complex. Crop emerging dorsally from the buccal complex as a heavily ciliated, thick-walled tube opening into the gizzard. Gizzard similar to that described from P. aperta though the gizzard plates are not equal nor do they possess the two attachment pits in their outer basal surfaces prominent in the latter animal. Gizzard opening posteriorly into a very short, ciliated stomach which, in turn, leads immediately into the digestive gland which is in the form of a long sac with one primary and several secondary lobes. Digestive gland in the immature animal occupying the major part of the body cavity within the posterior two thirds of the head shield, but restricted to the ventral half of the body by the overlying gonad in the mature animal. Intestine opening laterally on the left side of the stomach as a narrow ciliated tube then crossing the body cavity dorsally in a wide loop to the right side, extending down the mid-line of the body and eventually discharging into the right side of the mantle cavity. Unlike P. aperta, the digestive gland is restricted almost entirely to the region of the head shield, penetrating even in the largest specimens, only a very short distance into the visceral hump. There is no diaphragm.

Nervous System: Central nervous system (Fig. 3b) similar to that described for P. aperta though differing in detail. Cerebral, pleural and pedal ganglia lying in a similar relationship to each other as they do in the latter species though the cerebral commissure is proportionally very much shorter. Cerebral nerves, supplying

the Hancock's organs and the anterior part of the body, in the form of ganglia and, like those described in Pluscula cuica Marcus 1953, a member of the Philinoglossacea, having a distinct sheath. Eyes situated on a short optic nerve arising from the anterior face of the cerebral ganglia. Visceral loop very short and, as in P. aperta, supra-oesophageal ganglion joined to the right pleural ganglion. Infra-oesophageal ganglion joined to the visceral ganglion from which the genital and visceral nerves run posteriorly. Buccal ganglia lying immediately behind and ventral to the buccal complex and joined medially. Statocysts situated on the pedal ganglia but supplied with nerves from the cerebral ganglia having a single statolith.

Renoperigardial System: Kidney entirely confined to the visceral hump. It is a lobed sac lying predominantly on the right side of the body immediately above the nidamental gland mass of the reproductive system. It discharges into the mantle cavity near the anus. Heart situated on the right side of the body on the same level but anterior to the kidney to which it is connected by a short, well-defined renopericardial duct. Auricle and ventricle well developed, the aorta running forward from the latter alongside the gut.

Reproductive System (Fig. 3a) : Hermaphrodite gonad lying dorsally above the digestive gland, contained entirely within the head shield, composed of numerous follicles, some of which are concerned solely with the production of oocytes and some solely with the production of spermatozoa. Bulk of female portion of gonad situated antero-dorsally though a number of female follicles are also symmetrically arranged on either side at a slightly more ventral level. Major male portion of gonad restricted to its posterior dorsal region. Ventrally these specialised regions of the gonad discharge into a wide common atrium in which both ova and sperm occur imultaneously. From this atrium the hermaphrodite duct arises. The duct loops completely across the body to the right side then returns to the left where it turns sharply again and opens directly into the lumen of the albumen gland. This structure opens in turn into the histologically more complex mucous gland from which the efferent genital duct travels to the genital aperture on the right side of the mantle cavity. Shortly before reaching the genital aperture the efferent duct gives off a branch which widens into a prominent spermatheca which lies on the right side of the genital mass.

Although it is not impossible that the genital products actually follow the convoluted lumen of the nidamental gland mass, a detailed examination of the ciliation of the lumen of the different regions and the way in which these are connected to each other suggests that these products follow the shortest path to the outside through the central region of the gland mass. The secretions generated by the nidamental glands appear to come into contact with the ova within this central pathway. P. exigua differs in this respect from P. aperta where the secretions of these glands discharge on to the ova immediately before these are liberated to the outside.

Penis situated on the right side of the head in a muscular penis sheath opening a little to the right of the mouth in the anterior transverse portion of the lateral groove. Prostate gland in the form of a long, coiled tube, which is connected to the penis posteriorly. Seminal duct entering the body adjacent to the penial opening joining the anterior end of the prostate. There appears to be no specialised seminal groove connecting the seminal duct with the genital aperture along the right lateral

groove. There are several very narrow tracts of long cilia in this groove but these tracts are also present in the left lateral groove. In view, however, of the minute size of the lateral groove in these animals it may be that the several ciliated tracts present in the right groove all contribute to the forward movement of sperm.

A number of very small, but typically Philine type spawn masses (Fig. 3c), were recovered from the sand together with the adult P. exigua. The egg sac of these measured about 2mm in length and were anchored in the sand by a slender tail some 3mm long. The eggs filled the sac completely and were not arranged in the fine spiral commonly seen in the spawn masses of the larger species of the genus.

Mantle Cavity: Mantle cavity of P. exigua located beneath the visceral hump between the end of the foot and the caudal lobes, opening anteriorly on each side to the lateral grooves of the head shield. There is no gill but the strongly ridged roof of the cavity may function as a respiratory surface. Whole of the cavity ciliated and, where it opens posteriorly, the inner surface of the caudal lobes of the visceral hump are equipped with exceptionally long cilia forming a broad raphe across the posterior opening (Fig. 4b). Hypobranchial glands lying both in the posterior roof of the mantle cavity and in the caudal lobes, secreting a supply of mucus into the main ciliated channel. There is no osphradium.

In living P. exigua a large yellowish orange spot located beneath and anterior to the shell cavity is indistinctly visible through the epithelium of the visceral hump. In sections the spot is an empty sac connected to the roof of the mantle cavity by a short but well-defined duct (Fig. 4a and 4d). Where the duct opens into the sac it is surrounded by a distinct ring of a very darkly stained granular tissue. The function of this organ is unknown, but on the highest magnification available the tissue of which it is composed appears very similar to the retinal tissue of the animal's eye. It seems improbable that there should be a light-sensitive organ present at the posterior end of the animal and if living specimens can be obtained the nature of this organ will be investigated with the electron microscope. A sac-like gland similar to the above has been noted from other opisthobranchs. In Pluscula cuica, Marcus found a similar structure apparently having a glandular function. He reported that " the fundus is composed of big, nearly colourless secretory cells and supporting cells, and evolved by fine muscle fibres ". For this organ Marcus adopted the term "pallial gland" after Guiart (1901: 69-70) and although the lumen of the organ present in P. exigua is completely lacking the large gland cells it is reasonable to use the same terminology in this case, at least until a further study can be made.

Discussion

Although P. exigua differs in a number of morphological details from the larger species of Philine there is no doubt that it is a member of that genus. Only the pallial gland and the associated sense organ are particularly remarkable, and the former has been described on several occasions (Herding, 1932; Marcus, 1953), from members of the sand-dwelling Philinoglossacea, a group that although taxonomically remote from the Philinidae closely parallels the present species in size, in eternal form and in their restriction to a similar habitat.

Acknowledgments

I am grateful to the Royal Society of London for their invitation to participate in the 8.5.1. P. expedition and the South Pacific Research Programme Committee for granting funds which enabled me to do so. I thank Professor J. E. Morton of the University of Auckland for his constant encouragement and advice during the expedition and Dr M. C. Miller for his interest in this work.

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Mr D. A. Challis, Department of Zoology, University of Auckland, Auckland.