The Pallial Organs and Foot: Feeding and Cleansing Mechanisms.
When removed from the shell Stephopoma roseum is seen to be spirally coiled; the visceral mass is never irregularly vermiform as in Serpulorbis. The foot forms a stout plug-shaped column, surmounted by a very prominent operculum (Fig. 1 OP.). This is a thick chitinous disc, multiannular, and with each annulus fringed at its free edge with long multifid setae, figured in Text Fig. 1. The glandular regions of the foot are white in colour, forming a conspicuous area in front of the mouth. There are no pedal tentacles, but the front edge of the foot is produced into a median vertical process in front of the mouth, the pre-oral appendage discussed below. The rest of the foot and the exposed parts of the head are dark black or grey, and the trunk and pallial region whitish. The proboscis (Fig. 1 RO.) is short and bluntly rounded, jet black in colour, with the mouth a vertical slit at its tip. A pair of minute tubercles (TNT.) represents the cephalic tentacles, with small eyes at their outer bases. The pallial cavity forms a spacious chamber, and its contained organs may be conveniently considered in discussing the feeding process.
Stephopoma is a ciliary feeder on diatoms collected from the pallial current by the ctenidial filaments. The mechanism of feeding conforms to the fundamental type made familiar by the accounts of Yonge (1938) and other writers on ciliary feeding prosobranchs. There are, however, numerous differences in detail, and while most closely resembling Crepidula, Stephopoma is in some respects more
specialized than any of the previously known forms. The gill filaments (G.FIL.) are long, flexible, and rod-shaped. They are freely movable, and attached to the mantle for a short distance only, along the extreme acial side of the gill. They reach across the mantle cavity to the right to form a sort of temporary septum between ventral inhalant and dorsal exhalant chambers; (Text Fig. 2); but the whole gill is much less rigid than in Crepidula (Orton, 1912), where the filaments form a set of stiff rods. In Stephopoma there is a noticeable power of independent muscular movement. The separate filaments frequently bend and curve slightly, especially near the tips where the skeletal rods are vestigial and the intrinsic longitudinal muscles are well represented. The gill does not quite cover the hypobranchial gland (Fig. 5 HY. GL.), which is well developed, covering the right side of the mantle as a series of opaque white, transverse folds. The rectum opens by the anal papilla some distance behind the mantle margin. Immediately below the rectum is the ciliated genital furrow in the male—terminating simply, without a penis, and in the female, the glandular pallial genital duct. The renal organ opens on the mantle roof by a narrow slit, mesially to the rectum, rather far back.
Text Fig. 2—Stephopoma roseum. Diagrammatic view of the foot and head region,
part expanded and viewed from above, showing the course of the ciliary currents.
The setose crown of the operculum has been omitted. X. AP, pre-oral process;
CT, gill filament; EN, endostyle; EXH, exhalant region of the pallial cavity;
F.G, food groove; GL.F, glandular sole of foot; INH, inhalant region of pallial
cavity; OP, operculum (simplified); PA, mantle; REJ, lateral rejectory tract of
foot; RO, proboscis; SI, siphonal tubercle.
The mantle margin is entire, without inhalant siphon, and densely speckled with black. There is a single row of blunt papillae, repre-
senting a fringe of very short pallial tentacles. A powerful current is drawn into the pallial cavity on the left by the beating of the cilia of the gill. Such large particles as acutally alight on the pallial margin are quickly removed by fine, outward beating cilia. The remainder travel back along the line of the osphradium, being drawn obliquely to the right on to the frontal surface of the gill. The osphradium has the structure usual in primitive mesogastropods—a ridge overlapping on either side a line of sensory cells, and finely ciliated along its edges, which are black-pigmented. The length of the sensory zone is increased by close-spaced meanders and the osphradium extends the whole length of the gill. It is well situated for the important role suggested by Hulbert and Yonge (1937)—of determining the amount of sediment entering the pallial cavity. Between the asphradium and the gill axis lies a narrow glandular tract, the endostyle, serving for the supply of mucus in which are entangled the particles reaching the gill in the inhalent current. In Serpulorbis (Morton, 1951a) the endostyle is undeveloped; but its presence in Stephopoma is important owing to the virtual disappearance of the glandular areas on the gill filaments. The endostylar epithelium is of the type described by the writer in Struthiolaria (1951) and present also in Turritella: cigar-shaped glandular cells alternate regularly with tall, narrow, ciliated cells (50–60μ) keeping up a constant transverse beat towards the gill. Stephopoma has not—like Crepidula (Orton, 1914)—developed separate tracts of ciliated and glandular cells, after the manner of the unrelated pharyngeal endostyle of the lowest chordates.
The gill filaments possess the usual ciliary tracts (Fig. 6). The frontal cilia (FR.C.) are short but fast-beating, extending along the ventral aspect of each filament, facing the pallial cavity floor, and carrying mucus-bound particles direct to the edge of the gill. The lateral cilia (LAT.C.) are extremely long (40μ)—as in Crepidula, a good deal taller than the width of the filament itself. They lash dorsally between the filaments, and effectively strain off particles which are retained on the frontal side. Their metachronal beat is very distinctive, the rapid wave passing in opposite directions along the anterior and posterior sides of each filament. There is a tract of smaller and weaker abfrontal cilia (AB.C.) along the dorsal aspect of each filament, beating—like the frontals—towards the apex. The tip of each filament is equipped with a tuft of very tall (50μ–60μ) generally motionless apical cilia (AP.C.) whose functional role is discussed below. In transverse section (Fig. 6, a, b, c; Fig. 14) the gill filament shows a less specialised condition than in Crepidula: the slender skeletal rods remain—as primitively—close to the frontal side, and the respiratory area of thin cuboidal epithelium—though much reduced—is still present. The gland cells of the respiratory area are almost lost, and contribute but little of the mucus for the collection of particles. As well as from the endostyle, mucus is probably received from the hypobranchial gland in considerable amount. At frequent intervals the row of filaments is flexed upwards against the roof of the mantle cavity in close contact with the folds of the gland.
During feeding the filaments normally bend downwards towards the floor of the mantle cavity. Their tips are closely pressed together into the food groove, especially anteriorly where several filaments
generally overlap in a cluster (Fig. 4, G.FIL.). The food groove is a shallow gutter along the surface of the trunk. It is bounded on the right by a thin fold of ciliated and glandular epithelium. Passing towards the head it narrows considerably, and the bounding fold enlarges, being capable of much muscular movement. Its edge is often crenellated or frilled; the inner surface is uniformly ciliated. The fold curves, runs forward to terminate level with the mouth, just below the right tentacle (F.G.). The food groove cilia keep up a constant current passing forward all particles deposited by the gill filaments. The tip of each filament is rather expanded and bulbous, uniformly covered upon the frontal aspect with short terminal cilia (T.C.). These have a fast beat forwards across the surface of the filament, and when in contact with the food groove contents play an important role in moving food particles. The bristle-like apical cilia are kept perfectly motionless when the filaments are removed and examined. They are most typically observed in action as described below, when the anterior portion of the gill is protruded from the pallial cavity. But they probably also have some part in the forward movement of material in the food groove. Anteriorly the contents of the food groove are continually rotated by the lining cilia, and the terminal fold imparts a strong kneading action by muscular contractions. Finally a thick mucous cord, rotating in clockwise direction, is protruded from the opening of the groove for ingestion at the mouth (Fig. 4). Only the finest of particles, such as diatoms and flagellates, find their way into the food groove. Carmine or other foreign material entering the pallial cavity is quickly collected by the gill and swept away without entry to the groove.
The glandular portions of the foot in Stephopoma (Fig. 1, Text Fig. 2) are adapted for collecting and rejecting waste particles alighting near the head or carried out of the pallial cavity. There is no trace of the specialised pedal mucus gland described in “Vermetus” and Serpulorbis, nor of ciliated pedal tentacles. The gill alone is employed in food-collecting, and mucus traps are never put out from the foot. The original plantar surface of the foot now forms a convex pad (G.FT.) white in colour, situated between the margin of the operculum in front, and the mouth behind. It is finely ciliated and densely supplied with mucus glands. The anterior portion of the foot is narrowly constricted from the sole, forming the tall, papilliform, pre-oral appendage which stands up vertically in front of the mouth. Running forwards towards the operculum, around the margins of the sole, are two wide, shallow grooves (REJ.). They converge posteriorly at the base of the pre-oral appendage, and are greyish-black pigmented, bounded by muscular, somewhat crenellated edges. They serve as rejection tracts for unwanted particles from the neighbourhood of the mouth and from the debouchment of the food groove. Waste material is compacted into a rounded bolus, enclosed in mucus, and is rejected from the foot at the mid-line. A load of rejecta from time to time accumulates in the bristles of the operculum, and is ultimately swept away by the sudden retraction of the food, or the passage of the exhalant current.
The pre-oral appendage (AP.) is white in colour, very muscular and labile. It assumes a variety of shapes, being generally spatuli-
Fig. 1—Stephopoma roseum. The head and foot region of the fully expanded animal,
showing the ctenidial sweeping fringe and the course of the feeding and rejectory
Fig. 2—Pyxipoma weldii. The complete animal removed from
the shell and viewed from the right side.
Fig. 3—Pyxipoma weldii. The base of the operculum, viewed from below.
Fig. 4—Stephopoma roseum. Head region drawn from life, showing the action of the
radula in detaching a food bolus from the mucus cord in the food groove.
Fig. 5—Stephopoma roseum. Semi-diagrammatic transverse section through the trunk
and pallial cavity in front of the anus. Portions of two successive gill filaments
here appear in the same section.
Fig. 6—Stephopoma roseum. Gill filaments. a, b, c. Transverse sections of filaments,
near the base (a), at mid length (b), and at the apex (c). d, e. Ventral view of
tip of filament, showing apical cilia inert (d) and in action during food collection
or rejection of particles.
AB.C, abfrontal cilia; AP, pre-oral appendage; AP.C, apical cilia; B.P, opening of
brood pouch; CM, style caecum; CT, ctenidium; END, endostyle; E.SI, exhalant
siphonal appendage; F.G, food groove; FR.C, frontal cilia; F.BOL, food bolus;
G.FIL, gill filament; G.FT, glandular region of the foot; HY.GL, hypobranchial
gland; INT, middle region of intestine; K, renal organ; LAT.C, lateral cilia;
M.BOL, mucus bolus of material rejected from foot; OE, oesophagus; OP, operculum;
OS, osphradium; R, rectum; RA, radula; REJ, rejectory tract of foot;
RO, proboscis; SK.R, skeletal rod; SL, pallial slit; ST, stomach; T.C, terminal
cilia; TNT, cephalic tentacles.
Fig. 7—Female genital ducts and intestine viewed from the right side.
AL, albumen gland; CP, capsule gland; K, renal organ; MI, middle intestine;
OV, ovarian duct; RM, rectum.
Fig. 8—Stomach and Crystalline Style Caecum dissected from the dorsal aspect, showing
the course of the ciliary currents.
Fig. 9—Photomicrograph of transverse section of oesophagus, shortly before its opening
into the stomach.
Fig. 10—Photomicrograph of transverse section of the head, showing pharyngeal bulb,
eye (on left) and tips of anteriormost gill filaments (on right).
Fig. 11—Transverse section of style caecum and proximal portion of intestine.
Fig. 12—Photomicrograph of transverse section of a single tubule of the digestive gland.
Fig. 13—Photomicrograph of transverse section of stomach, through gastric shield,
sorting area and digestive diverticulum.
Fig. 14—Photomicrograph of gill filaments in transverse section.
CM, style caecum; C.S., ciliary sorting area; DT, dorsal typhlo [ unclear: ] ole; DV, digestive
diverticulum; EY, eye; F, crescentic fold referred to in text; G.FIL, gill filament;
I.GR. groove of proximal intestine; M.I., middle intestine; OD, odontophore;
OE, oesophagus; SH, gastric shield; ST, crystalline style; VT, ventral typhlosole.
Figs. 15, 16, 17—Pyxipoma weldii. Embryo shell removed from brood pouch, showing
operculum closing aperture (16) and part open (17).
Fig. 18—Stephopoma nucleogranosum. South Australia. Nuclear portion of mature
Fig. 19—Stephopoma roseum. Embryo shells.
Fig. 20—Stephopoma roseum. Milford Reef, Rangitoto Channel. Embryo enclosed in
capsule membrane, removed from pallial cavity.
Fig. 21—Stephopoma roseum. Milford Reef, Rangitoto Channel, Embryo at creeping
stage, after emergence from capsule membrane, removed from throat of adult
shell. CT, cephalic tentacle; F. foot; F.G, terminal portion of food groove;
GF, gill filaments; MO, mouth; OP, operculum; PA, mantle; PG, anterior pedal
Fig. 22—Pyxipoma weldii. A single row of radular teeth, marginals omitted on right.
Fig. 23—Stephopoma roseum. A single row of radular teeth.
form with the edges at times incurved to form a sort of temporary tube. Its function was difficult to determine exactly, but it appears to be employed in connection with both feeding and waste rejection. It is frequently curved to the left towards the opening of the food groove, or held in front of the mouth as a spoon-like lobe, perhaps assisting the prehension of the mucus cord by the radula. In the related Pyxipoma (Fig. 2) where the food groove termination is curved round to the mid-line, and the bolus carried straight to the mouth, the pre-oral appendage is not developed. Material from the food groove that is not ingested at the mouth, falls immediately on the lateral rejection tract of the right side of the foot. It is thence quickly carried forward to the base of the operculum, and this is also the case with large foreign particles extruded from the mantle cavity. When carmine or carborundum is introduced by the inhalant current, the gill is temporarily lifted free of the food groove. The particles are rapidly carried across the gill by the frontal cilia, embedded in mucus from the endostyle. The now activated apical cilia carry the mucus string forward and it is immediately swept out of the pallial cavity with the exhalant current. The hypobranchial gland appears to play only a minor role in the rapid elimination of waste. The pre-oral appendage assists in the rejection of smaller particles, such as finer grades of carborundum. Particles are carried by cilia up the middle line of the posterior side of the appendage, and round the tip, which is temporarily indented to allow material to pass over the top. They are now carried downwards along the anterior aspect, diverging to right or left sides, to be carried across the glandular cushion of the foot, and finally swept forward along the lateral rejectory tracts.
Apparently the animal may feed normally for a considerable time with the foot part retracted into the shell. The operculum does not then entirely close the shell, but rests with its bristles pressed against the shell edge; the inhalant current thus passes through a sieve-like mesh of bristles, which may thus have a function similar to the pallial tentacles of Turritella, in guarding against the entry of excessively large particles. The operculum is slightly smaller in diameter than the shell tube, and the animal may retreat within the shell, with the flexible bristles bent forwards to allow backward retraction of the foot.
On the right side of the foot, to the right of the food groove opening, is a structure corresponding to the exhalant siphonal tubercle of Turritella. It forms a short, stout, triangular papilla, backwardly pointed, and often slightly curved (E. SI.). It is apparently not ciliated, though traversed by a shallow groove running from base to tip. From its base a fold of integument runs back to the bounding fold of the food groove, along which the sperm groove runs in the male. Though the papilla is present in both sexes, it may well serve to guide the outward current of sperm released by the aphallic male. In addition, especially in the part retracted animal, it curves backward so as almost to enclose a circular opening to the right of the food groove, through which the exhalant current issues from the mantle cavity. The rudiment of the siphonal appendage is present at an early stage in the creeping embryo, together with the food groove fold (Fig.
21, F.G.). At the same stage the anterior edge of the foot is narrow and squarish, very labile and well ciliated. It is already reminiscent of the pre-oral appendage to which it gives rise in the sessile adult.
Stephopoma roseum kept alive in the laboratory was occasionally observed to employ the gill in a second type of food collecting action (see Fig. 1). Although difficult to induce regularly under artificial conditions the details of this process are extremely interesting. When the animal is fully extended, the head and foot project a good distance from the shell, and the anterior part of the gill—about one fourth its total length—is protruded from the pallial cavity by the extension of the mantle skirt. The projecting filaments radiate to form a wide, semi-circular fringe of flexible cirri, which is able to be drawn through the water in a manner somewhat like the sweeping net of a cirripede, though at longer intervals and in a more leisurely manner. At regular intervals the ctenidial fringe is curved back sharply over the rim of the mantle, so that the filament tips are bent down close to the sides of the shell. Almost immediately there follows a rapid recovery sweep, the filaments resuming their original spreading position (Fig. 1). By supplying carmine particles to the projecting portion of the gill, the nature of the ciliary currents can be detected. The mucus secretion from the endostyle is especially copious, and is carried out rapidly to the tips of the filaments by the frontal cilia. The fast-lashing lateral cilia meanwhile temporarily cease beating. This effectively prevents the mucus supply being swept inwards between the filaments and lost. Particles deposited on the gill filaments are swept to the tips, entangled in mucus, which rapidly accumulates as a continuous rope, passing from filament to filament along the frontal side of the gill. It is now that the long, generally inert apical cilia come into play (Fig. 6, e). With a slow uniform beat, they pass the mucus rope around the edge of the fringe towards the head region. The beat of the apical tufts, as illustrated in Fig. 1, is thus backwards in direction in this part of the gill, from the anteriormost to the more posterior filaments, as far as the point where the gill emerges from the mantle cavity. The fate of the collected particles may differ. Large indigestible carmine masses are cast off the edges of the gill on to the rejection tract of the foot, which carries them forward and discards them. Finer particles, however, appear to be deposited actually within the food groove, as they reach those filaments of the gill which still remain dipped into the groove. In this way diatoms and other suspended organisms are added to the food collected by the gill from the inhalant pallial current, as described above. In natural conditions it is probably the stimulus of particles alighting on the gill that induces the abundant secretion of mucus for the sweeping net mode of feeding. Such a method of food collecting is supplementary to the more usual employment of the pallial ciliary currents. It was not possible to determine to what extent relatively the animal relies upon one method or the other, especially as Stephopoma is extremely shy in the aquarium tank, and as a rule remains withdrawn into the shell, or with the aperture about half opened. The development of a ctenidial sweeping net has not previously been recorded in a mollues; such an adaptation is extremely effective in enabling a sessile animal thickly clustered together to
exploit to the full its available feeding area. Stephopoma is thus to be regarded as ecologically equivalent to the sessile cirripedes and the tubicolous serpulid polychaetes.