Biol. J
' . Linn. SOC.,3, p p . 329-342. With 3 plaies and 5 fisures
December 1971
The diurnal rhythm and tidal rhythm of feeding and digestion
in Ostrea edulis
BRIAN MORTON
The Marine Laboratory, Portsmouth Polytechnic,
Ferry Road, Hayling Island, Hampshire"
Acceptedfor publication April 1971
Observations on the rhythms of the edible oyster Osireu edulis show it to have both a diurnal
rhythm as well as a tidal rhythm of feeding and digestion. There is also a semi-lunar rhythm
which is the resultant of the diurnal and tidal rhythms.
CONTENTS
.
Introduction
Materials and methods
The diurnal rhythm .
The tidal rhythm
Discussion
.
Summary.
Acknowledgements
References
.
.
.
.
.
.
.
.
. ..
.
. .
. .
. .
..
PAGE
329
330
333
333
339
340
341
341
INTRODUCTION
As early as 1920 Nelson (1925, 1933) showed that Crassostrea virginica does not feed
during the latter part of the night and that at sunrise, before active feeding has begun, the
crystalline style is usually thin or may even be absent. On the flood tide when the oysters
are feeding, the style is large and firm, but when the tide has ebbed and digestion is far
advanced, the style is reduced to a soft amorphous mass of jelly. However, the concept
of bivalves as forms in which the processes of feeding and digestion are simultaneous
and continuous has long been accepted by most zoologists, and accordingly the work of
Nelson has been largely overlooked. Purchon (1968) quotes Jergensen (1955) as
questioning the statement by Nelson that Crassostrea may cease to filter sea-water at low
tide, and Loosanoff & Nomejko (1946) suggest that adverse conditions may have
developed locally at the time of low tide. Elsewhere they found that Crassostrea
virginica filters water and feeds at all times of day and night regardless of the state of
the tide.
Loosanoff & Nomejko (1946) found that Crassostrea virginica kept its valves open for
90 yi of the time when living under natural conditions, whilst Hopkins (1937) reported
* Present address: Department of Zoology,University of Hong Kong.
329
330
B. MORTON
that at naturally occurring temperatures Ostrea lurida was open for 20 hours per day
and C . virginica for 10-14 hours.
Marceau (1906, 1909) demonstrated that many bivalves, including Ostrea, possess
rhythms of adductor activity and quiescence.
Brown (1954) and Brown et al. (1956) have recently shown that C. sirginica possesses
rhythms of activity that can be related to day and night and also to the tidal cycle.
Summation of these two rhythms results in a semi-lunar rhythm.
More recently rhythms of feeding and digestion have been described for Lasaea rubra
(J. E. Morton, 1956), Dreissena polymorpha, Anodonta cygnea, Cardium edule and
Macoma balthica (B. S . Morton, 1969, 1970a, b c).
In the light of this new evidence it seemed desirable to reappraise the situation in
0. edulis.
MATERIALS AND METHODS
In the early summer of 1970 the Ministry of Agriculture and Fisheries Research
Laboratories at Burnham-on-Crouch, Essex, kindly supplied large numbers of
Ostrea edulis.
These oysters had been relaid in November 1967 as two-year-old seed oysters in the
Brickfield Bight region of the river Crouch and were, when supplied, grade 1 five-yearolds. In the Crouch the oysters were covered by approximately 10 feet of water at low
tide and 25 feet at high tide. The animals were collected one afternoon and delivered to
Portsmouth early the next day and immediately transferred to an outdoor 2000-gallon
sea-water tank filled with fresh sea-water. The bottom of the tank was covered by one to
two inches of sand and after 12 months of constant replenishment by sea-water had
accumulated a healthy fauna and flora such as might be found on any sandy sublittoral
shore. Twenty-four trays were lowered into the tank, each containing eight oysters.
This facilitated the removal of eight oysters at a time without disturbing the remainder.
The oysters were thus living in an artificial environment which resembled their natural
habitat as closely as possible.
Two days after their arrival from Burnham eight oysters (in a single tray) were
removed from the experimental tank every hour for a total of 24 hours and treated as
follows :
(1) Removal of upper shell valve with an oyster knife.
(2) Measurement of the pH of the fluid in the mantle cavity.
(3) Insertion of a pipette into the oesophagus of the oyster and removal of the
stomach contents and recording of the following:
(a) colour (yellow or clear white);
(b) PH;
(c) viscosity;
(d) constituents.
(4) The crystalline style was removed and the following recorded:
(a) colour (yellow or cream);
(b) texture (solid or gelatinous);
(c) length and greatest width (to nearest 0.5 mm);
( 4 PH.
DIURNAL AND TIDAL RHYTHMS IN OSTREA EDULIS
331
( 5 ) A section of the digestive diverticulum of the right caecum was removed and the
following recorded :
(a) colour (light brown or dark brown);
(b) pH (of four of the animals);
(c) histological structure of the digestive tubules (of four of the animals).
I .
I
1
I
2
Time (mid
I
3
I
4
FIGURE
1. Calibration of glucose-water solutions of known viscosity plotted against the time
taken for a standard drop of solution to run down a glass slide inclined 5" from the vertical.
Each point represents the mean of five readings. The best fitting rectilinear regression has
also been plotted.
were ground up with four or five drops of neutral de-ionized water and the pH of the
resulting fluid measured.
The viscosity of the stomach contents was estimated by allowing a standard drop
(from the microcapillary electrode of the pH meter) to run down a glass microscope
slide inclined from the vertical by 5" and registering the time taken for the drop to run
from the top to the bottom. This experimental technique was calibrated using different
glucose-water mixes of known viscosity. Figure 1 shows the results obtained from the
332
B. MORTON
FIGURE2. Kymograph records of the activity of four specimens of Ostrea edulis. T h e times
of night and day are also shown.
DIURNAL AND TIDAL RHYTHMS IN OSTREA EDULZS
333
calibration and the log-linear relationship. After estimating viscosity in this way a drop
of 4% formolsaline was added to the slide and temporary preparations made of the
stomach contents for inspection after completion of the experiment.
Pieces of the digestive diverticula of four of the eight oysters were fixed at hourly
intervals in alcoholic Bouin-Dubosq, sectioned at 6 pm and stained in either Heidenhain’s haematoxylin and light-green or Ehrlich’s haematoxylin and eosin.
Over a period of four or five months other oysters, from the same locality (i.e.
Burnham-on-Crouch, Essex) were attached by their lower shell valves to a glass block
and by their upper shell valves to a waxed thread attached to a writing lever and placed
in a two-gallon tank through which fresh sea-water constantly flowed. Opening and
closing movements of the shell valves were recorded by the writing lever on a smoked
kymograph drum rotating at a speed of one revolution per week.
THE DIURNAL RHYTHM
Recordings of the adductor activity of a large number of specimens of Ostrea edulis
revealed a rhythm of adductor activity and relative quiescence that is diurnal. Figure 2
shows recordings of the activity of four specimens of Ostrea.
During daylight hours the animal is very much more active than at other times and
phasic contractions of the adductor muscle recur with a frequency ranging from one
to five adductions per hour (Table 1). At night the contractions are less frequent and
relaxation of the adductor muscle allows the shell valves to part and the animal gapes
for long periods. At this time the adductions have a frequency that is only between
0.1-2.3 per hour.
These recordings agree closely with those of Brown (1954) for 0. virginica but,
contrary to his observations, reveal an overt rhythm and not just a statistical indication
of a rhythm.
THE TIDAL RHYTHM
Results
Analysis of the data obtained from the experiments has revealed that Ostrea edulis
possesses a rhythm of feeding and digestion that can be correlated with the tidal cycle at
Burnham-on-Crouch calculated from the published tidal predictions for this region
(Reed’sNautical Almanac and Tide Tablesfor 1970) (Fig. 3).
T h e p H of the sea-water in the experimental tank did not vary significantly during
the experiment and had a mean p H of 7.97 (Fig. 3 S.W.).
The p H changes in the mantle cavity and alimentary canal
T h e pH of the fluid in the mantle cavity did not vary significantly over the experimental period (Fig. 3 M.F.) and possessed a mean pH of 7.39. Similarly the p H of the
stomach fluids (Fig. 3 S.F.) showed only slight variation, but this did not vary significantly from the mean p H of 5.798.
T h e p H of the crystalline style and to a lesser degree of the digestive diverticula
did, however, vary over the 24 hours (Fig. 3 C.S., D.D.) and in unison with the tidal
B. MORTON
334
cycle. The pH of the style fell on two occasions prior to high tide. These two falls in
pH of the style coincided with slight rises in the pH of the digestive diverticula. At
other times the pH of the style was high (i.e. greater than pH 7) but two smaller falls
in pH also occurred about low tide.
Table 1. The relative number of major phasic adductions that
occurred in each of eight animals over a four-day period during
night and day
Animal
Date
No.of
adductions
per hour
(night)
A
7 Mar. 1970
8 Mar. 1970
9 Mar. 1970
10 Mar. 1970
22 Mar. 1970
23 Mar. 1970
24 Mar. 1970
25 Mar. 1970
3 Apr. 1970
4 Apr. 1970
5 Apr. 1970
6 Apr. 1970
5 Apr. 1970
6 Apr. 1970
7 Apr. 1970
8 Apr. 1970
26 Apr. 1970
27 Apr. 1970
28 Apr. 1970
29 Apr. 1970
2 May 1970
3 May 1970
4 May 1970
5 May 1970
20 May 1970
21 May 1970
22 May 1970
23 May 1970
30 May 1970
1 Jun. 1970
2 Jun. 1970
3 Jun. 1970
0.10
2.20
1*05
0.75
2.30
1*05
1*05
0.05
0.70
0.20
0.70
0.50
1.80
1.30
0.80
0.50
0.35
0.70
1.10
1-45
1.20
0.95
0.80
1.25
0.50
1.10
0.65
0.75
0.60
0.55
1.15
0.80
B
C
D
E
F
G
H
No. of
adductiom
per hour
(day)
2.50
4.35
3.10
3.95
4.00
2.50
4.95
3.80
3.00
2.75
1.80
2.65
1.55
2-30
4.10
2.35
3.00
1.95
3.15
4-45
2.90
3.50
2-45
3.20
2.35
0.95
1.05
1-50
2.35
3.20
3.80
2.40
The pH changes in the digestive diverticula were not so marked, but as a general
rule it appeared that the pH fell on an ebbing tide and rose on the rising tide.
The mean pH of the style and digestive diverticula were 6.80 and 6.46 respectively,
the digestive diverticula being the most acid organs in the gut of 0. edulis.
The crystalline style
The volume of the style (calculated as the volume of a cone) was the factor which
changed most noticeably over the course of the experiment. Twice, coinciding with
DIURNAL AND TIDAL RHYTHMS IN OSTREA EDULIS
335
three hours before high-tide, the style almost disappeared. At these times the mean
volume of the style fell to 3-4 mm3. At other times the style was a large solid rod with a
mean volume of up to 25 mm3. On both tidal cycles the volume of the style seemed to
decrease slightly just before low tide. Similarly the colour and texture of the style varied
over the two tidal cycles (Fig. 3). The style was solid and cream-coloured when large,
but gelatinous and yellow when small.
The stomach jluid
T h e viscosity of the stomach fluid varied systematically over the 24 hours during
which the experiment was performed, having a mean viscosity of approximately two
poises for the greater part of the time but rising sharply to five poises just after high
tide at the time when the style had dissolved. Similarly the colour of the stomach
contents varied, being cream-coloured on the falling tide but yellow on the rising tide.
T h e most noticeable changes that took place were in the composition of the stomach
fluid. T h e stomachs of those animals examined on the falling tide contained large
amounts of ingested material (Fig. 3 ; Plate lA,B,D,E). Mucous food strings
(Plate 1A,D) were observable immediately after high tide but later were found to have
broken up (Plate 1B,E). On the rising tide the contents of the stomachs were very
different, being composed of large numbers of fragmentation spherules derived from
the digestive diverticula (Fig. 3 ; Plate lC,F). Between these extremes, two to three
hours after low tide the stomach contained very little solid material.
At the time of feeding the stomach contents of the oysters contained large amounts
of unidentifiable detritus, sand grains, sponge spicules, diatoms, algal cells, nematodes,
barnacle cyprids, whole copepod nauplii and fragments of these, gastropod radula teeth,
unidentified crustacean fragments and unidentified eggs. By far the most easily recognizable, but not the most numerous, constituents of the stomach fluids were the diatoms.
Although it is not suggested that the diatoms are an important food of the oyster, it was
considered worthwhile identifying them. T h e following identifications are based upon
descriptions and figures of British diatoms by Hendey (1964).
Amphora sp.
Biddulphiu alternans (Bailey)
Cocconeis sp.
Coscinodiscus radiatus Ehrenberg
Diploneis didyma (Ehrenberg)
Diploneis littoralis (Donkin)
Nitzschia sp.
Navicula abrupta (Gregory)
Navicula crucigera (Wm. Smith)
Navicula palpebralis de Brebisson
Navicula peregrina (Ehrenberg)
Pinnularia ambigua Cleve
Pleurosigma strigosum Wm. Smith
Rhuphoneis amphiceros (Ehrenberg)
Rhaphoneis surirella (Ehrenberg)
Rhizosolenia sp.
Skeletonema costatum (Greville)
The digestive diverticula
As noted earlier the pH of the digestive diverticula varies slightly over the course
of the tidal cycle and at certain times fragmentation spherules are observable in the
stomach in large numbers. T h e fragmentation spherules are derived from the digestive
diverticula.
Permanent stained sections of the digestive diverticula show that their structure
varies with the rhythm of the tide.
23
336
B. MORTON
Night
09
I
II
I
Cream
Style
(colour)
I
I
I
I
l
13
I
I
i
.
15
I
I
,
17
I
I
19
I
I
1
I
"
'
1
21
23
I
I
1
1
1
I
I
I
1
01
[
1
'
I
'
1
,
I
1
03
I
I
05
I
07
I
,
1
1
4
.
I
I
,
1
1
1
1
2
1
1
1
1
2
2
2
1
1
1
1
'
Yellow
Solid
I l l , !
Style
(texture)
Tubule
form
I
I
1
1
I
.
1
1
1
1
2
23
2
2
1
1
.
I
I
2
2
2
2
2
2
2
2
2
1
2
2
~
I
1
1
1
1
1
,
Gelatinous
2 3
23
23
2
2
3
3
3
3
3
34
3
456456671
6 4 1 1
45 45617 1
3 6 1 1
2
1
2
1
233
3 3 1 1 1
2 3 34 4561671
1
2 3
3 4 4 16 2
1
2 3 3 4 4 5 4 5 1 1 1 2
1
2
2
DIURNAL AND TIDAL RHYTHMS IN OSTREA EDULIS
337
On the rising tide the tubules are newly formed (Figs 3 and 4, condition 1; Plate
2B); the darkly staining basiphil cells can be distinguished from the lighter digestive
cells, which have not yet begun to absorb food material. Some basiphil cells may possess
cilia. At high tide and in the earlier part of the falling tide the tubules are absorbing
food material (Figs 3 and 4, condition 2; Plate 2C); the digestive cells are swollen
with many food vacuoles. The basiphil cells possess long cilia (Plate 3A). One or two
hours before low tide, initiated by the production of fragmentation spherules from the
tips of the digestive cells the tubules have begun to break down (Plate 3 C) and the loss
of the cilia from the basiphil cells (Figs 3 and 4, condition 3 ; Plate 2D). At low tide,
breakdown of the tubule is nearly complete (Figs 3 and 4, condition 4; Plate 2E). Very
rapidly the cells of the parent tubule break up yet further (Plate 2F) to produce a tubule
in which the cells are very low (Figs 3 and 4, condition 5 ; Plate 2G) and digestive
cell and basiphil cell are hard to distinguish. At this stage numerous amoebocytes with
assimilated material may be observed in the haemocoele surrounding the tubules
(Plate 3B,D). Differentiation of the cells of the tubule in condition 5 ultimately results
in the formation of a tubule in condition 1, ready to receive more food material from the
stomach. New tubules are apparently formed by the basiphil cells of the parent tubule
budding to form a cluster of cells (Figs 3 and 4, condition 6; Plate 2H), which ultimately
develop a lumen (Figs 3 and 4, condition 7; Plate 2A) and finally develop into a newlyformed tubule (condition 1).
Correlation
Figure 5 suggests a schematic representation of the feeding and digestive processes
of Ostrea edulis based upon the observed changes in structure and function of the various
regions of the gut.
The oyster feeds at high-tide and from high-tide to low-tide the stomach is filling
with food. This event is preceded on the rising tide by the total dissolution of the crystalline style which increases the viscosity of the stomach contents (Fig. 3) and releases
various enzymes (Yonge, 1926). The food thus enters the stomach at a time when it
contains large amounts of digestive enzymes. After preliminary extra-cellular digestion
in the stomach, food material unsuitable for further absorption and digestion is passed
to the mid-gut. At this time the stomach is relatively empty. Material suitable for
absorption and intra-cellular digestion is passed to the light-brown digestive diverticula
FIGURE
3. A diagram correlating day and night, the diurnal rhythm of adductor activity and
quiescence, the rhythm of the tide, the pH changes in the experimental tank (S.W.),mantle
fluid (M.F.), crystalline style (C.S.), digestive diverticula (D.D.), stomach fluid (S.F.), the
volume of the style, viscosity of the stomach fluid, colour of the digestive diverticula, stomach
fluids and style, the composition of the stomach contents, texture of the style and the form of the
tubules of the digestive diverticula.
All points on the graphs represent the mean of eight readings, except for the p H of the digestive
diverticula where the points represent the mean of four. The vertical bars in the histograms
represent observations, and the position of the bars when referred to the base line indicate
the number of animals that possessed either of two characteristics. Where the vertical bars
are not equal to eight indicates that those animals could not fulfil either of the two characters:
e.g. a style could not be yellow or cream if it was not present. The numbers associated with tubule
form represent the condition indices given to the tubules of four animals fixed at the same
time. The numbers are referrable to Fig. 4.
B. MORTON
338
FIGURE
4. A diagrammatic representationof the various tubule conditions encountered in the
experiment. The numbers 1 to 7 represent the condition indices and are explained in the
text.
Feeding
\
Feeding
Waste out
\
'
Breakdown
.
Absorption in D U
Reformotion
Refor motion
Breakdown
1
Assimilation
+
Assimilatiorr
Reformation
t
Assimilation
FIGURE
5. A schematic representation of the tidal rhythm of feeding and digestion in Ostrea
edulis.
DIURNAL AND TIDAL RHYTHMS IN OSTREA EDULIS
339
during the succeeding rising tide. At this time, and at this time only, the digestive
tubules are in a condition suitable for this process to occur. After intra-cellular digestion
has been completed the digestive diverticula (which are now a dark-brown colour) break
up passing assimilated material to the rest of the body (perhaps in amoebocytes as
originally suggested by Yonge (1926)), and waste material back to the stomach in
fragmentation spherules. At the time the fragmentation spherules arrive in the stomach
the style is being re-formed (i.e. on the ebbing tide). The arrival of fragmentation spherules in the stomach, turns the colour of the stomach contents from cream to yellow and
has a slight dissolutory effect upon the style, also turning it yellow. However, since the
style is still being formed in the style-sac, the effect of the fragmentation spherules is
only slight and it can be seen from Fig. 3 that the style only dissolves slightly at low
tide and is able to reform. Once formation of the style ceases, however, the fragmentation spherules quickly act upon the style to dissolve it. Owen (1955) suggested that the
fragmentation spherules may break up and liberate extra-cellular digestive enzymes in
the stomach. This is almost certainly true, but what is more important, disintegration
of the fragmentation spherules is responsible for dissolution of the style.
It has previously been noted that the digestive diverticula are the most acid organs
in the gut of the oyster, but that the pH of the stomach fluids is lower. Since the pH of the
style is always higher than that of the stomach contents then the fragmentation spherules
must be very acid, probably more acid than the diverticula as a whole and these dissolve
the style and interact with the style material and food to produce a solution that is both
acid and buffered. The changes in pH of the style are probably caused by the action of
the fragmentation spherules upon a relatively neutral substance.
These findings agree closely with the figures and interpretation put upon them by
Yonge (1926) of the pH of the stomach contents of the oyster, but not with his recordings
of the pH of the style and digestive diverticula.
There can be no doubt that the processes of feeding and digestion in 0. edulis are
rhythmic and are based upon the tidal cycle.
DISCUSSION
Crussostreaoirginica (Brown, 1954) possesses a tidal cycle of adduction which during
the first two weeks under constant conditions possessed maxima in synchrony with the
time of high tide in the native habitat of the oysters, but thereafter the rhythm shifted
its phase relations to display maxima at the times of lunar zenith and nadir. The specimens of 0.edulis used in this study also displayed a tidal rhythm that could be correlated
with the time of high tide in their native habitat.
Brown (1954) has also shown that C. oirginica possesses a diurnal rhythm-the same
is true for 0. edulis. It has been suggested by Brown (1954) and Nicol(l960) that the
simultaneous occurrence of these two rhythms, diurnal and tidal, results in semi-lunar
cycles having a frequency of 14.8 days, at which intervals the diurnal and tidal cycles
are in the same phase relative to one another. It may well be that the summation of these
two rhythms to produce a semi-lunar rhythm in 0.edulis may account for the semi-lunar
occurrence of oyster larvae in the plankton of the rivers Roach and Crouch (KnightJones, 1952) and explain how breeding is synchronized in this species.
340
B. MORTON
Of major importance to 0. edulis, however, is the tidal cycle since it is this regularly
occurring rhythm of the environment that is responsible for synchronizing the feeding
and digestive processes of the individual. The rhythm of feeding and digestion in Ostrea
bears a very close resemblance to that possessed by Cardium edule (B. S . Morton,
1970b) in that both animals feed at high tide and the food is digested later, largely
during the period of low tide. C. edule is, however, an intertidal form and the exposure
to the animal caused by the ebbing tide results in much more noticeable changes.
Since the animal is incapable of replenishing the water in its mantle cavity at low tide
the pH of the mantle fluid falls at this time, due to a build-up of carbon dioxide. Ostrea,
on the other hand, living permanently submerged can filter the water (but not ingest
food) continuously and there is no build-up of carbon dioxide. The total dissolution
of the crystallinestyle in Ostrea with every tidal cycle also enables the animal to keep the
pH of its stomach contents buffered. In Cardium,however, and in Dreissenapolymorphu
(B. S. Morton, 1969) the style only partially dissolves and the pH of the stomach
contents fluctuates widely but still regularly.
The tidal rhythm in Ostrea is remarkably similar to the tidal rhythm possessed by
Lasaeu rubra (J. E. Morton, 1956; McQuiston, 1969) and in both forms it seems as
though the sporadic release of fragmentation spherules into the stomach from the
digestive diverticula plays a major role in the dissolution of the style and the primary
extra-cellular digestion of food.
The digestive diverticula of Ostrea undergo a wide variation in structure and function
throughout the tidal regime and are closely comparable with those of other lamellibranchs e.g. Lusaea (J. E. Morton, 1956), Dreissena, Anodonta, Cardium and Macoma
JB. S. Morton, 1969, 1970a,b,c).
Yonge (1926) did not observe cilia arising from the basiphil cells of the digestive
tubules, but in this study it has been shown that the basiphil cells do sometimes possess
cilia, but only occasionally. At other times the same cells possess another function, i.e.
the formation of new tubules. The digestive cells (as originally suggested by Yonge)
are responsible for the intra-cellular digestion of food.
The occurrence in 0. edulis of a mode of life in which the processes of feeding and
digestion are rhythmic and related to the tides confirms the earlier work of Nelson
(1925, 1933) on C. oirginica, and shows that Nelson probably was correct in asserting
that the style regularly dissolved and re-formed with every tidal cycle. It is also suggested that the demonstration of a rhythmic mode of feeding and digestion in these
forms necessitates a change in currently accepted scientific thought regarding the
mode of feeding of the Bivalvia as a whole.
SUMMARY
(1) Ostrea edulis possesses a diurnal rhythm of adductor activity and quiescence.
(2) 0. edulis also possesses a tidal rhythm of feeding and digestion the phases of
which can be related to
(a) the feeding habits of the individual;
(b) the extra-cellular digestive processes in the lumen of the stomach correlated
with
DIURNAL AND T I D A L RHYTHMS IN O S T R E A EDULZS
341
(i) the secretion and total dissolution of the crystalline style;
(ii) the arrival in the stomach of fragmentation spherules from the digestive
diverticula.
(c) T h e intra-cellular digestive process in the digestive diverticula correlated
with the development, absorption, breakdown re-formation and regeneration of the digestive tubules.
It is concluded that Ostrea edulis is a discontinuous feeder, a fact which substantially vindicates earlier work Crassostrea virginica.
ACKNOWLEDGEMENTS
During the course of this investigation the writer has been supported by a research
associateship awarded by Portsmouth Polytechnic.
1 am greatly indebted to D r Peter Russell, without whose help the large number of
observations on so many animals over 24 hours could never have been accomplished,
and also to Professor R. D. Purchon, Chelsea College of Science and Technology,
University of London, who kindly read the first draft of this manuscript and made
many valuable suggestions and criticisms.
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M. F., WEBB,H. M. & RALPH,C. L., 1956. Persistent daily, monthly and
27-day cycles of activity in the oyster and quahog. J . exp. Zool., 131: 235-262.
HENDEY,N. I., 1964. A n introductory account of the smaller algae of British Coastal Waters. Part. V .
Bacillariophyceae (diatoms). London : H .M .S.0.
HOPKINS,
A. E., 1937. Experimental observations on spawning, larval development and setting in the
Olympia oyster, Ostrea lurida. Bull. U S . Bur. Fish., 48: 439-503.
JBRGENSEN, C. B., 1955. Quantitative aspects of filter feeding in invertebrates. Biol. Rew., 30: 391454.
KNIGHT-JONES,
E. W., 1952. Reproduction of oysters in the rivers Crouch and Roach, Essex, during
1947,1948 and 1949. Fishery Invest., Lond., 18: 1 4 8 .
LOOSANOFF,
V. L. & NOMEJKO,
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342
B. MORTON
EXPLANATION OF PLATES
PLATE
1
The stomach contents of specimens of Ostrea edulis. A,B, Mucous food chains; B,E,partially digested
food material; C,F, fragmentation spherules. Magnification: A,D, ~ 5 0 B,E,
;
~ 1 0 0 C,F,
;
~200.
PLATE2
The digestive tubules of Ostrea edulis showing the various stages of formation, absorption and breakdown
that occur over the tidal cycle. B,Condition 1 ; C, condition 2; D, condition 3 ;E, condition 4 ; F and G,
condition 5; H, condition 6; A, condition 7 (for explanation see text). Magnification: A 4 , approximately
~ 2 0 0H,
; x500.
PLATE
3
The digestive tubules of Ostrea edulis. A, Cilia arising from a cluster of basiphil cells; B,D, amoebocytes
containing assimilated material; C, fragmentation spherules being budded from digestive cells.
Magnification: A,C, x800; B,D, ~ 2 0 0 0 .
Bio1.J. Linn. S o c . , 3 (1971)
Plate 1
(Facing p . 342)
Bio1.J. Linn. SOC.,
3 (1971)
B. MORTON
Plate 2
Bio1.J. Linn. Soc., 3 (1971)
B. MORTON
Plate 3