539
Notes on the Mechanism of Food Movement in the Gut
of the Larval Oyster, Ostrea edulis
By R. H. MILLAR
(From the Marine Station, Millport, Isle of Cumbrae, Scotland)
SUMMARY
The histology and mechanism of food movement in the stomach of the larval oyster
are described. Cilia line the stomach, except the left wall, roof, and upper part of the
right wall, which bear the smooth gastric shield. The diverticula contain non-ciliated
absorptive cells and ciliated non-absorptive cells. A slender muscle passes round each
diverticulum. Food is rotated in the stomach by the style, and also turned over in the
sagittal plane. Particles are drawn into the diverticula and returned to the stomach by
the rhythmic expansion and contraction of the diverticula.
INTRODUCTION
UCH is now known of the structure, histology, and functioning of the
gut in the adult oyster and other lamellibranchs. In the larval oyster,
also, the general structure and function have been described (Horst, 1883;
Yonge, 1926; Erdmann, 1935), but the existing accounts need some additions
and corrections, especially with regard to the manipulation of the food once
it has reached the stomach. The present paper deals with the larva of Ostrea
edulis L., which was studied during breeding experiments at the Marine
Station, Millport.
M
METHODS
In order to follow the movements of particles within the gut, larvae were
kept in sea-water to which was added titanium dioxide (Acheson Colloids
Ltd.), or cells of the flagellate Isochrysis galbana Parke. Larvae were also fixed
in Bouin, in the expanded state, by first using propylene phenoxytol (Owen,
1955) as a narcotizing agent. Paraffin sections were cut at 5//. and 10/1. and
stained with Heidenhain's haematoxylin, followed by acid fuchsin or orange
G as counterstain.
STRUCTURE OF THE GUT
The gut has already been described and illustrated (see figures in Yonge,
1926, and Erdmann, 1935). The long oesophagus leads into the anterior end of
the stomach, and from the posterior end of the stomach the style sac projects
backwards. From the posterior end of the right side of the stomach the midgut passes round the end of the style sac and turns forward to make an
anterior loop lying to the left of the stomach. The rectum runs almost straight
back to the anus. The diverticula lie one on each side of the stomach and
open separately into its floor.
[Quarterly Journal of Microscopical Science, Vol. 96, part 4, pp. 539-544, December 1955.]
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Millar—Notes on the Mechanism of Food Movement in the
The oesophagus is uniformly ciliated and of simple structure, but the
stomach is more complex. At its anterior end immediately above the opening
of the oesophagus is an area with long cilia, and the lower part of the right
wall also bears cilia. On the upper part of the right wall, on the roof, and on
the whole of the left wall, however, the epithelium of the stomach is modified
and instead of having cilia is covered by the smooth gastric shield (fig. i). The
existence of this structure in the larva has already been noted by Erdmann
food moss
qastric shield
anterior loop
of midqut
midqut
style sac
openinq of
riqht diverticulum
muscle round
riqht diverticulum
riqht diverticulum
oesophaqus
FIG. I. Gut of larval oyster seen from the right; partly reconstructed from sections. The
right wall of the stomach and part of the right wall of the right diverticulum have been cut
away. Arrows show the direction of movement of the food and the rotation of the style.
(1935), but he stated that the shield was on the right and dorsal walls of the
stomach. He deduced its position from a reconstruction of sections (see his
Abb. 5, p. 20), but the true situation of the gastric shield on the left and dorsal
walls can be determined by using as landmarks the opening of the midgut on
the right, and also the anterior loop of the midgut which lies to the left of the
stomach. In Erdmann's own figure (Abb. 18, Taf. 3) the shield is seen to be
on the same side as the anterior loop of the midgut, i.e. on the left. The gastric
shield is formed of the specially thickened cuticular border of the epithelial
cells. Part at least of the left ventral border of the shield is further thickened
and inrolled as a distinct ridge (see fig. 1). In a transverse section this ridge
appears as a hook-like structure projecting into the lumen of the stomach. The
cells underlying the gastric shield are in other respects similar to those of the
rest of the stomach and of the style sac. The style sac is uniformly ciliated but
Gut of the Larval Oyster, Ostrea edulis
541
the cilia of the dorsal surface are stouter than those of the ventral surface
and there appears to be a small apical area of the sac which lacks cilia. The
style, lying within the sac, projects forward into the stomach. A small central
strip on the floor of the stomach is ciliated and on each side of this strip lie
the single openings to the diverticula. Each diverticulum in the larva is simple
and sac-like, unlike the much divided structure of the adult. The cells of its
walls are of two kinds, absorptive and ciliated (fig. 2). Most of the cells are
absorptive, and these are cubical with lightly staining cytoplasm containing a
few vacuoles. Material within these vacuoles is presumed to be absorbed food,
as Yonge (1926) has shown that absorption occurs exclusively in the diverticula.
The nuclei of these cells, often deformed by pressure of the food vacuoles,
absorptive cell
FIG. 2. Part of the wall of a diverticulum, in section.
contain only scattered chromatin and no large nucleolus. The remaining cells
occur in small groups called by Yonge (1926) crypts of young cells. These
cells have more deeply staining cytoplasm than the absorptive cells. They are
also distinguished by their nuclei which have a large nucleolus and are spherical, there being no vacuoles in the cytoplasm to cause nuclear deformation.
Although cilia have not been seen with certainty on these cells, their apical
ends bear rows of granules deeply staining with iron haematoxylin and having
the appearance of basal granules. It is therefore highly probable that they are
the ciliated cells of the diverticula, especially as cilia have been demonstrated
by Owen (1955) on similar cells in the tubules of the adult diverticula. In the
larva, however, cilia are not responsible for the movements of food particles
into and out of the diverticula, these movements resulting from muscular
activity. Fig. 3 represents an obliquely transverse section through a larva, and
shows a slender strand of muscle fibres passing round the outside of each
diverticulum in an antero-ventral to postero-dorsal direction. The strand of
muscle seems to come into contact with the posterior retractor muscle of the
velum, but its relationship to that muscle is obscure. There may possibly be
542
Millar—Notes on the Mechanism of Food Movement in the
other fine strands of muscle round the diverticula, but no others were seen.
Both the midgut and the rectum are ciliated, and at the entrance of the midgut
to the stomach the cilia are especially large.
FIG. 3. Obliquely transverse section through a larva, to show the muscles round the
diverticula.
MECHANISM OF FOOD MOVEMENT
Food particles collected by the cilia of the velum and mouth are passed by
the oesophageal cilia into the front of the stomach. Here they accumulate
round the end of the style as a conical mass which is rotated by the action of
the style revolving under the influence of the cilia of the style sac. The cilia
of the right wall of the stomach probably also help to rotate the food. In all
oyster larvae which I have examined the food mass revolved in a clockwise
direction as viewed from the anterior end; that is, the movement of particles
is up across the right wall and down across the left wall. It was often noticed
that rotation of the food mass was slowed down or stopped, as if by an
obstruction, in the lower left part of the stomach. This obstruction is, in fact,
the ventral ridge of the gastric shield. Yonge (1926) states that in some larvae
which he observed the rotation was clockwise and in others anti-clockwise,
Gut of the Larval Oyster, Ostrea edulis
543
although constant in any one larva. As mentioned above, I have seen only
clockwise rotation, and anti-clockwise rotation might be rendered difficult by
the shape of the ventral ridge of the gastric shield, but clockwise rotation is
apparently adapted to that shape. The gastric shield is perhaps useful in
breaking up food organisms as they are pressed against it in rotating, although
such a process hardly seems necessary with the small delicate flagellates which
are known to constitute the food of the larvae (Cole, 1937; Bruce, Knight, and
Parke, 1940). The shield may also serve, as in the adult, to grind the end of
the style.
In addition to rotating about the axis of the style, the food mass is also constantly turned over by a sort of rotation in the sagittal plane. This is accomplished by the cilia of the ventral strip of the stomach driving particles forward
and by the long cilia of the anterior end of the stomach passing them up to
the dorsal side of the food mass (fig. 1).
Food particles pass from the stomach into the diverticula, not by ciliary
activity, but by the rhythmic expansion and contraction of the diverticula
themselves, brought about by the action of the slender muscles which pass
round them. This pulsation was seen only when the larva was in the swimming
position with the velum protruded and never when the body was retracted
between the shells. In different larvae the rate of pulsation varied between 5
and 22 contractions per minute, and was usually between 18 and 21. When
the diverticula dilate food particles are drawn in, and when they contract they
are expelled to rejoin the rotating food mass in the stomach. Larvae seen from
the dorsal side showed that the diverticula do not pulsate in unison, but
alternately. This may be advantageous by preventing undue pressure-changes
within the stomach which might result from the simultaneous action of the
two diverticula. It may also help each diverticulum to expand if its muscular
relaxation coincides with the increased pressure due to the contraction of the
other diverticulum. But it is difficult to decide to what extent pressure-changes
of this kind would be transmitted from one to the other.
Particles are drawn off from the posterior end of the stomach by the cilia
at the mouth of the midgut. As there appears to be no sorting mechanism in
the larval gut, other than the exclusion of large particles by the small diameter
of the mouth and oesophagus, it is a matter of chance whether material drawn
off into the midgut and thence passed to the rectum has been in the stomach
for a short or a long time, and therefore to what extent it has been subjected
to digestion.
DISCUSSION
The rotation of food round the end of the style and its turning over in the
sagittal plane ensure thorough mixing and uniform treatment of all material
taken in. The direction of rotation which I have observed is the same as that
recorded in adult lamellibranchs (Nelson, 1918; Yonge, 1926, 1949, 1951a,
19516; Owen, 1953; Allen, 1954), and the position of the gastric shield is
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Millar—Food Movement in Gut of Ostrea
similar. There is therefore continuity of structure and function from the larva
to the adult.
The larval diverticula also have a certain resemblance to those of the adult,
although much simpler in form. Similar absorptive and ciliated cells occur,
and the function of the diverticula is evidently comparable in both stages of
the oyster. But there may be important differences in the mechanism by
which particles are exchanged between the stomach and the diverticula. Owen
(1956) observed no contraction of the muscles which envelop the tubules of
the diverticula of the adult oyster, although he suggests that the system of
longitudinal fibres may 'from time to time, contract slowly to empty the contents of the tubules . . .'. He concludes that solid particles and liquid are
passed into the tubules by the ciliary activity of the ducts, in which there is
also a compensating flow in the opposite direction. In the larva there are no
ducts to the diverticula, which open directly into the stomach, and the cilia
of the diverticula probably serve only to agitate particles already present in
the lumen. The pumping action of the diverticula produced by their own
muscles is a much more efficient way of emptying and refilling these sac-like
structures than a ciliary mechanism would be. It is uncertain how far the
simple and active muscles of the larval diverticula are comparable with the
complex and apparently inactive system of the adult.
REFERENCES
ALLEN, J. A., 1954. Quart. J. micr. Sci., 95, 473.
BRUCE, J. R., KNIGHT, M., and PARKE, M. W., 1940.
J. Mar. biol. Ass.
COLE, H. A., 1937. Fish. Invest. Lond., 15, 1.
ERDMANN, W., 1935. Wiss. Meeres. Helgoland, 19, (3), 1.
HORST, R., 1883. Bull. U.S. Fish. Comm., 2, 159.
NELSON, T. C , 1918. J. Morph., 31, 53.
OWEN, G., 1953. J. Mar. biol. Ass. U.K., 32, 85.
1955- In the press.
1956. In the press.
YONGE, C. M., 1926. J. Mar. biol. Ass. U.K., 14, 295.
1949. Phil. Trans. B., 234, 29.
1951a. J- Mar. biol. Ass. U.K., 30, 387.
19516. Unif. Calif. Publ. Zool., 55, 395.
U.K., 24, 337.