20ol.J. Linn. SOC.,49, pp. 255-269. With 11 jgures
November 1970
Defaecation in some macrothricid and chydorid cladocerans, and
some problems of water intake and digestion in the Anomopoda
GEOFFREY FRYER
Freshwater Biological Association, The Ferry House, Far Sawrey, Ambleside,
Westmorland
Accepted for publication January 1970
Former inaccuracies in the description of the gut of the cladoceran Acantholeberis are corrected
and it isthereby shown that this animal has a method of defaecation unique within the Macrothricidae. Other cladocerans including certain chydorids and daphnids also exhibit anal drinking
which, whatever its other functions, would appearto prevent loss of digestion products and to increase the efficiency of food utilization in animals which may retain food in the gut for less than
30 minutes.
CONTENTS
Introduction
.
Previous statements relating to the alimentary canal of Acantholeberis curwirostris .
Morphology of the alimentary canal of A. curvirostris
The process of defaecation in A . curvirostris .
Defaecation in Eurycercus lamellatus
Entry of water into the gut and its movements
.
Some implications of copious drinking .
Summary.
.
Addendum
.
Acknowledgement .
References
.
Abbreviations used in figures
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PAGE
255
256
257
259
261
262
266
268
268
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269
269
INTRODUCTION
The present investigations began when it was realized that most statements referring
to the anatomy of the posterior end of the alimentary canal of the macrothricid
anomopod Acantholeberis curvirostris (0. F. Muller) are incorrect, and that several
published illustrations are equally erroneous. Because of this the functional significance
of the true arrangement, which is related to a mechanism of defaecation which is
unique within the Macrothricidae, has not been appreciated. A similar mechanism is,
however, shared by members of the Chydoridae belonging to the genus Eurycercus and
probably also by members of the genus Leyd+ia. This mechanism is described.
During its elucidation observations were made on the intake of water via the anus and
on its movements within the gut. These movements, here described for the first time,
may have far reaching implications in relation to the digestion and absorption of food,
but a detailed consideration of these physiological aspects of the phenomenon has not
been attempted.
19
255
256
G. FRYER
PREVIOUS STATEMENTS RELATING TO THE ALIMENTARY
CANAL OF ACANTHOLEBERIS CURVIROSTRIS
Early accounts of the alimentary canal of A. curvirostris are not always explicit.
Thus Muller (1776) gave the original description of this species without illustration,
but in 1785” provided a figure which shows an unlooped gut without a diverticulum.
The gut is not mentioned in the text. From the time of Schodler (1846), however,
several investigators, often in monographs or much-used taxonomic works, either make
specific statements or provide illustrations of the alimentary canal, or both. Often
both the descriptions and illustrations are erroneous.
In a remarkable study of AcanthoZeberis, Schodler (1846) refers to the gut as having
a single coil posteriorly, and his illustrations clearly portray a posterior loop and no
diverticulum. Similarly Norman (1864) refers to the gut of Acantholeberis as being
‘furnished with a loop near the anus’ and such a loop is one of the most obvious features
of his figure of A. curvirostris. No diverticulum is shown. Furthermore he at that time
regarded the alleged presence of a loop as being one of the principal differences
between this genus and Macrothrix. Likewise Hellich (1877) states that ‘Der Darm
tragt keine Blindsicke und bildet erst im Postabdomen eine grosse Schlinge’, and
provides a passable illustration in which, as he describes, the gut is endowed with a
posterior loop and leads to the anus without giving off a diverticulum. The meticulous
Lilljeborg (1900) is equally categorical, stating that ‘Der Darmkanal bildet im Hinterrumpfe und im vorderen Hinterkorper eine Schlinge; blinddarmahnliche Anhange
fehlen’, and his figures are suggestive of a loop and not of a diverticulum. Likewise
Birge (1918) refers to the intestine as ‘convoluted, the loops lying in great part in
post-abdomen’ and his figure clearly shows a loop and no diverticulum. Brooks (1959)
in the second edition of this work, repeats Birge verbatim and uses the same figure.
Furthermore, in both editions this statement (shown below to be erroneous), supported
by an inaccurate illustration, is employed in the key to identity. The illustration in
the excellent key of Scourfield & Harding (1941 and subsequent editions) also shows
a looped gut. Manuilova (1964) copies Lilljeborg’s figure and says ‘Gut with loop’
(translated from Russian).
In fact the gut is not looped and does have a diverticulum. That this is so is stated
or illustrated by certain authors, though seldom convincingly. Thus Wagler (1937)
correctly states ‘Mitteldarm am Ende mit blindem Anhang’,yet reproduces Lilljeborg’s
figure which shows a looped gut with no diverticulum. Herbst (1962) also includes
‘Mitteldarm mit blindem Anhang’ in his diagnosis, which is correct, but his sketch,
while not very revealing on this point, gives the impression of a looped gut. Of the
other important monographers SrBmek-HuBek (1962) correctly, but rather crudely,
portrays a diverticulum but does not indicate whether a loop is present. The two are
not necessarily mutually exclusive.
All the major monographs or keys are therefore either incorrect, or at best ambiguous
on this point. At least one author, however, (Gurney 1915) correctly illustrates the
arrangement but does not refer to the point in the text of what is a non-anatomical
* There appear to have been two editionsof this work, for the copy available to me bears the date 1792
yet the title, pagination and plate numbers are the same as the classical publication of 1785.
T H E CLADOCERAN GUT AND DEFAECATION
257
paper. That the situation has been so frequently misinterpreted means that the
functional significance of the true arrangement has never been appreciated.
MORPHOLOGY OF T H E ALIMENTARY CANAL OF
ACANTHOLEBERIS CURVIROSTRIS
The gut of Acantholeberis has no loop but is provided posteriorly with a large
diverticulum. This arises within the post-abdomen from what is morphologically the
ventral, but functionally the dorsal, side of the extreme posterior end of the mid-gut.
AW
CM
FI
\
NC
PM
MG
\
DSC
FIGURE
1. Longitudinal section through the post-abdomen and posterior end of the alimentary
canal of Acantholeberis curvirostris to show the nature and location of the diverticulum. The
section, which is cut a little to the observer’s side of the rectum, is of an animal that has recently
defaecated and into whose water-filled diverticulum food is just beginning to pass from the posterior end of the mid-gut. The arrow indicates the direction in which the faecal ribbon is
ejected. The inset shows, more highly magnified, part of the posterior wall of the diverticulum
and two of its muscle strands. (For key to lettering see page 269.)
Its location, form and extent, as seen in longitudinal section, are indicated in Fig. 1.
Distally it rises towards the overlying mid-gut. When the diverticulum of the living
animal is filled or almost filled with food, its volume is such that it can be seen from
above, as indicated in Fig. 10.
The posterior (morphologically dorsal) wall of the diverticulum (PW) is lined
internally with cubical epithelial cells (Figs 1to 3) which sometimes appear somewhat
swollen. Arching over this portion of the wall like half hoops of a barrel are nine or
ten separate muscle strands (MS) scarcely to be seen in Fig. 1 but of which two are
shown in the inset. These are very fine and striations have not with certainty been
seen. The anterior wall (AW) lacks the epithelium of cubical cells and consists essentially of a basement membrane which is invested with numerous extremely fine circular
G. FRYER
258
muscle fibres. On the inner face of this wall a few delicate peg-like cells or projections
from cells are present (Fig. 2). The circular muscles of both walls insert on an endoskeletal element (E), which barely qualifies as an apodeme, and which is continuous
with a more extensive endoskeletal system (E') which helps to support both the
diverticulum and mid-gut and suspend them in the haemocoele (Figs 2 and 3).
MG
E
'AD
3
FIGURES
2 to 5. 2. Transverse section through the diverticulum and extreme hind end of the midgut of Acantholeberis cumirostris. 3. Transverse section through the tip of the diverticulum to
show the accessory diverticula. 4. Section adjacent to that shown in 3 to show the wall cells of
the distal portion of the diverticulum in face view. 5. Transverse section through the distal
region of the post-abdomen and rectum adjacent to the anus. This is a thick slice viewed from
the proximal end of the post-abdomen. The bases of the claws (C) appear as a result of deep
focussing.
At its blind extremity the diverticulum is provided with a pair of accessory diverticula
(AD) whose location is shown in Fig. 1. Histologically the few cells which line these
(Fig. 3) are not greatly dissimilar from those which line the posterior wall of the
diverticulum proper, and their staining reaction to Mallory's stain and to Masson's
trichrome stain (the only two employed) is the same. Histochemical tests have not,
however, been carried out. A noteworthy feature of the diverticulum, whose significance
is apparent when its mechanical operation is understood, is its complete lack of dilator
muscles.
T H E CLADOCERAN GUT AND DEFAECATION
259
The rectum (Figs 1 and S), which is suspended by a complex system of fibrils (F),
is provided with powerful circular (constrictor) muscles (CM) and an array of dilator
muscles (DM). At the extreme posterior end of the mid-gut, just before it meets the
rectum, there is, in a morphologically dorsal position, a number of dark staining cells
(Fig. 1, DSC) of unknown function. Adjacent to these and in the vicinity of the rectum
are what appear to be neurosecretory cells, but the nature of these is not proven.
The wide space shown ventrally at the extreme posterior end of the mid-gut in
Fig. 1 is not an artifact and can be seen clearly in the living animal, especially in
individuals that have taken coloured solutions into the gut lumen as described below.
Here delicate membranes (M), entirely independent of the peritrophic membrane,
and evidently freely permeable to water and certain solutes, ensure that the faecal
ribbon lies eccentrically within the lumen of the extreme posterior end of the mid-gut.
THE PROCESS O F DEF-4ECATION IN A. CURVZROSTRIS
The distribution of food in the alimentary canal of an individual that has just
defaecated and completed the series of events that immediately succeed this act is
shown in Fig. 6. At this stage the rectum is closed to the passage of faeces. This does
FIGURES
6 to 10. Diagrammatic representation of the filling of the diverticulum and of the act
of defaecation in Acantholeberis cumirostris. Just after defaecation the diverticulum contains no
faeces (6). Faecal matter passes into the diverticulum as feeding continues (7) and eventually
fills it (8). The contents of the diverticulum are then ejected via the rectum (9). 10 shows how,
when the animal is viewed from above, the swollen diverticulum is visible beneath the mid-gut.
G. FRYER
260
not, however, prevent the ingress of water via the rectum by means of occasional
gentle antiperistaltic movements (see below). Ingestion of more food causes the whole
column of food to pass along the alimentary canal. The most posterior portion, unable
to proceed through the rectum, gradually moves into the diverticulum (Fig. 7). This
process continues until the diverticulum is completely full of particulate material
(Fig. 8). Completion of this process is the presumed stimulus for several actions.
Activation of the necessary muscles causes the post-abdomen to be swung ventrally
and backward, the rectal dilator muscles contract and the circular rectal muscles relax,
thereby opening the rectal passage, and the dorsal, and probably also the ventral,
muscle fibres of the diverticulum contract, thereby expelling the contents of the
diverticulum, whose only route is through the rectum, to the exterior (Fig. 9). That
DF
EC
R
FIGURE
11. Diagrammatic representation of an early stage of the filling with faeces of the
diverticulum of Acuntholeberis cumirostris, showing also (EC) the erroneously described and
illustrated course that the faecal ribbon has been supposed to follow. This is here indicated by a
dashed line. Later stages in the filling of the diverticulum are indicated by the dotted lines.
portion of the material that was first to enter the diverticulum is the last to leave. The
swing of the post-abdomen ensures that the faecal ribbon is ejected at some distance
from the region from which food and the respiratory stream are derived. Immediately
after discharge of the faecal ribbon vigorous anal drinking takes place, about ten to
twelve gulps being usual.
The entry of faecal matter into the diverticulum is somewhat more complex than is
indicated in this outline account and certain points require elaboration. When, almost
immediately after defaecation, material begins to pass into the diverticulum it does so
as a ribbon whose diameter is determined by the diameter of the mid-gut from which
it came and by the investing peritrophic membrane. This passes into the diverticulum,
following a curved course and being pressed against the anterior (muscular) wall.
The faecal ribbon advances alongside this wall until it can go no further (Fig. 11), a
process which usually takes about three minutes, but as little as one minute in a rapidly
THE CLADOCERAN GUT AND DEFAECATJON
261
feeding individual. At this stage there is therefore a wide fluid-filled space between
the faecal matter and the posterior wall of the diverticulum. It is at this stage and a
little later that it is particularly easy to imagine that the ribbon passes behind (or over)
the posterior end of the mid-gut as a loop which continues to the rectum, and the
effect is greatly enhanced by the fact that at this stage there is no food in the rectum.
The course erroneously illustrated by several authors is indicated by dashed lines in
Fig. 11 (EC).
Continuous passage of material into the diverticulum now causes the end of the
ribbon to spread out and fill the distal portion, the delicate peritrophic membrane
being ruptured in the process. This distended mass then gradually fills the remaining
space, displacing water as it does so. Successive stages in this process are indicated
by dotted lines in Fig. 11. Eventually the entire diverticulum is filled, and it is then
that defaecation takes place. In an animal lying free, almost always the entire contents
of the diverticulum are discharged. On one occasion a small quantity of material
remained adjacent to the posterior wall. This has also been observed in an animal
lying on a slide, but here conditions are abnormal. Because faeces pass through the
rectum, whose diameter is less than that of the diverticulum, the length of the ejected
ribbon is considerably greater than the length of the diverticulum.
The time taken to fill the diverticulum varies according to the intensity of feeding
and also according to the kind of food being ingested. Undisturbed individuals of
Acantholeberis will often feed almost continuously if supplied with their regular
food-flocculent organic detritus-collected from the habitat in which they are living.
One such individual, kept at room temperature, was timed as it fed in this way, scarcely
moving over a period of more than two hours other than to move perhaps one body
length to a new food depot or to adjust its position slightly. Timed from the first act
of defaecation observed, it defaecated ten times in 132 rnin 46 sec, the intervals being
19 min 11 sec, 16 rnin 10 sec, 12 min 55 sec, 14 rnin 49 sec, 15 rnin 27 sec, 16 rnin 1 sec,
11 min 53 sec, 15 min 28 sec, and 10 min 52 sec (average 14 min 45 sec). Feeding
was continuing uninterrupted when observations were discontinued. Carmine particles
taken into the alimentary canal about 3 rnin 30 sec to 3 rnin 40 sec before the first of
these acts of defaecation, passed into the diverticulum some minutes prior to the third
discharge of faeces, at which they were voided, and remained in the gut for approximately 39 minutes. In another individual carmine particles reached the extreme
posterior end of the mid-gut within approximately 20 minutes of entering it from the
oesophagus. On some occasions, therefore, certain particles remain in the gut for no
more than about 20 minutes and probably sometimes for less. Further, the diverticulum is sometimes filled more quickly than recorded above: on one occasion the
process took only 3 min 45 sec.
As a very rough approximation the full diverticulum holds about half the contents
of the mid-gut-which is much more than is apparent when the animal is viewed
from the side.
DEFAECATION IN EURYCERCUS LAMELLATUS
While the situation in Acantholeberis (a monotypic genus) is apparently unique
within the Macrothricidae, other members of which family lack a diverticulum, at
262
G. FRYER
least two chydorid genera, Eurycercus and Leydigia,have a similar simple diverticulum.
I n all the several other chydorid genera investigated either a tubular organ, or a
glandular organ, or (Alona &nis Leydig) a modified glandular organ, opens into the
rectum, and no diverticulum is present (Fryer, 1969).
In its essentials the diverticulum of Eurycerw ZumeUutus 0. F. Muller is similar to
that of Acantholeberis. The method of defaecation also proves to be similar in both,
though there are small differences. In Eurycercus, as in Acantholeberis, faecal matter
is pressed against the anterior wall as the diverticulum fills. Here, however, the
diameter of the faecal ribbon is greater in proportion to that of the diverticulum than
in Acantholeberii, there is no ‘curlingover’ of the end of the faecal ribbon, and discharge
of the faeces ensues shortly after the ribbon has begun to press on the distal portion
of the diverticulum.
While in AcanthoZeM it is only material that has passed into the diverticulum that
is eliminated at defaecation, in Eurycmm a portion of material from the extreme
posterior end of the mid-gut is also discharged. The amount involved is considerably
less than that contained in the diverticulum and is ejected before the diverticular
contents, but some mixing seems to take place during discharge. As,in Acantholeberis
anal drinking takes place immediately after defaecation, but the number of gulps seems
always to be fewer-only three or four usually being seen. This is, however, difficult
to ascertain precisely as the process can only be studied satisfactorily in animals which
are feeding and are therefore free to move, and Eurycerw almost invariably dashes
away immediately after defaecation. In one instance an individual watched under very
favourable conditions was seen to defaecate, and no anal drinking was seen.
Although the feeding mechanism of Ley&ia @d@i Schodler has been studied
(Fryer, 1968) no serious attention was at that time given to the mechanismof defaecation
and as living material has latterly been unprocurable it has not been possible to check
whether, as seems probable, this is similar to that of Acanthleberis and Eurycercus.
ENTRY OF WATER INTO THE GUT AND ITS MOVEMENTS
Fox (1952), who has discussed the observations of earlier workers, has reported
continuous and rhythmic anal drinking in many, but not all, of the small crustaceans
which he observed, and also reported that in certain larger crustaceans anal drinking
preceded defaecation. He suggested that the prime purpose of this activity is to serve
as an enema ‘stretching the gut-wall muscles until they contract’ and thereby inducing
defaecation. He also showed convincingly that water was not taken in for respiratory or
osmotic purposes and suggested that it was also unconnected with the maintenance
of turgor.
Although in neither Acantholeberis nor Eurycercus is anal drinking so obvious as it is
in, for example, Daphnia, such drinking nevertheless occurs, as is readily observed by
immersing animals for a few minutes in solutions of dyes which do not stain the gutwall. Coloured water then enters the gut and its movements can be followed. For a
brief period immediately after defaecation water is pumped vigorously into the gut
via the rectum, but even in animals that have not defaecated, water enters, and its
inflow can be observed in individuals which have previously taken in coloured water,
THE CLADOCERAN GUT AND DEFAECATION
263
though the antiperistaltic movements of the rectum that are responsible are easily
overlooked. That this inflow of water does not act as an enema in Acuntholeberis and
Eurycercus is suggested by the fact that defaecation apparently invariably follows the
complete filling of the diverticulum with faeces in undisturbed animals, and that the
event can be predicted with confidence by watching this process even though, as the
feeding rate is not constant, defaecation occurs at irregular intervals.
If disturbed, Acuntholeberis sometimes discharges faeces before the diverticulum is
full-as when a specimen is placed on a slide-but this does not appear to be so in
undisturbed individuals. One observation is, however, at variance with those made on
feeding animals. An attempt was made to ascertain whether individuals with little or
no food in the gut would go through the motions of defaecation. Starved animals tend
to retain a little food at the posterior end of the mid-gut for several hours even though
the diverticulum is empty. Such individuals are much less easy to observe without
interruption than are feeding animals as they have no incentive to remain in one place.
One such individual was, however, seen to swing the post-abdomen and then gulp
water via the anus, suggesting that the diverticulum had been emptied. At present
this cannot be reconciled with what has been repeatedly observed in feeding animals.
Whatever the purpose of the anal drinking that takes place between two acts of
defaecation, and which seems not to be for distending the gut as a stimulus to this act,
the copious gulps taken by Acantholeberis immediately after defaecation seem most
reasonably interpreted as a means of restoring gut turgor, and hence turgor of the
body as a whole. An amount equal to about half of the particulate matter contained in
the mid-gut is discharged at each act of defaecation, and if the momentarily empty
diverticulum were to be refilled with liquid derived from that which surrounds the
food in the mid-gut a loss of turgor would be inevitable. Because Acuntholeberis has
an open blood system this loss of turgor would be transmitted to the body as a whole,
and it is obviously desirable that such a reduction of hydrostatic pressure be avoided.
This is done by vigorous anal drinking of water which refills-and physically reflatesthe diverticulum. Reflation of the diverticulum in a series of stages, each corresponding
to the intake of a gulp of water, has been clearly seen in individuals which defaecated
while lying on their side on a microscope slide. Such vigorous drinking is not to be seen
(or must be very infrequent) at other times. The same applies to Eurycercus though here
the number of anal gulps is fewer after defaecation-perhaps because, relative to gut
(and body) volume, a smaller amount of faeces is discharged. Such a rapid restoration
of turgor by the physical intake of water via the rectum is not at variance with Krogh's
statement (1939) that in Duphniu (and therefore probably in these animals) hydrostatic
pressure is only a small fraction of the osmotic pressure. As defaecation in Eurycercus
follows the complete filling of the diverticulum with faeces, exactly as in Acuntholeberis,
it is again difficult to believe that the gentle anal drinking which is almost always
taking place is responsible for the initiation of this process.
Fox (1952) has discussed the fate of the water which enters the gut of certain small
crustaceans by both mouth and anus and adduced evidence to show that most of it
passes through the gut wall into the haemocoele-which inevitably means copious
excretion. There is an unresolved problem here. While the full course of the excretory
tubule of the maxillary gland of certain anomopod cladocerans has been followed in
264
G . FRYER
sectioned material (I have been able to do so even in a species of Moina of which only
formalin-fixed material was available) all attempts to trace the duct in Eurycercus have
indicated that it ends blindly. Well-fixed material of this large chydorid, studied for
purposes unrelated to this investigation, never revealed an exit (Fryer, 1963). While
this may be a misleading conclusion-perhaps due to the firm closure of the aperture
in fixation, though I do not believe this to be so-the point merits mention.
While it is difficult accurately to measure the amount of water taken into the gut
over a given period of time, the fact that a diverticulum is present at least indicates the
minimum quantity taken in posteriorly between each act of defaecation. Immediately
after defaecation vigorous anal drinking fills the diverticulum with water. Thus an
amount of water equal to the volume of the distended diverticulum and roughly equal
to half the volume of the particulate matter in the mid-gut is taken in. This is gradually
replaced by faecal matter, but there is no evidence that any of it ever leaves the gut at
either end during this process. On the contrary, extra water enters as can be seen in
animals that have taken coloured water into the diverticulum and posterior end of the
mid-gut. This does not pass out between acts of defaecation: more water enters and
the coloured water moves anteriorly along the gut. Thus between each act of defaecation
an amount of water greater than the volume of the distended diverticulum is taken
into the gut via the anus and presumably passes through its walls.
Fox (1952) reported oral intake of water by Daphnia hyalina Leydig at a rate of
about 24 gulps/minute and had the impression that more water is taken in through
the mouth than through the anus. My own observations on the movements of coloured
fluids in the gut of Acantholeberis, Eurycercus, Daphnia magna Straus, D. longispinu
0. F. Miiller, and (a few observations only) D. hyalina galeata Sars reveal, however,
that more water enters via the anus than via the mouth. If individuals are immersed
for a few minutes in a solution of Light green a considerable amount of water is often
taken in posteriorly while little, or none at all, enters via the mouth. In all cases the
coloured fluid moves anteriorly along the mid-gut to its anterior end and when, as in
Eurycercus and Daphnia, anterior caeca are present, it eventually enters these.
The following observations document more precisely the movement of water within
the gut and are relevant to problems discussed below. Individuals of A. curvirostris
were placed in water coloured either by Light green or Nigrosin for three to five
minutes, passed through clean water, and transferred to a dish in which they were
provided with organic detritus as food. These were found to have taken coloured fluid
into the gut especially, and sometimes apparently exclusively, via the anus. Subsequently, although any liquid taken in at either end of the gut must have been water,
the intensity of the colour increased anteriorly and decreased posteriorly. The time
sequence for one individual immersed for about three minutes in a solution of Light
green was as follows. After removal there was only a trace of green anteriorly but the
liquid at the posterior end of the mid-gut and in the partly faeces-filled diverticulum
was intensely green. During the next 30 minutes or so food (and water) was taken in
orally and the animal defaecated at least twice-with the inevitable loss of some green
liquid on the first occasion for the faeces do not form a solid mass. Apart from losses
at defaecation, the green colour gradually disappeared posteriorly, not because it was
evacuated, but because the liquid in the gut was moved anteriorly by antiperistalsis
THE CLADOCERAN GUT AND DEFAECATION
265
and replaced posteriorly by further anal drinking. Eventually a conspicuous green
region occupied approximately the anterior ‘arch’of the alimentary canal. This persisted
for more than two hours, being still intense after 90 minutes. In other cases coloration
was still marked about three hours after ingestion and traces remained for about four
hours. That this coloration is due to liquid in the gut and not to staining of the gut wall
is evident from the way the coloured region moves along the alimentary canal, but was
proved by the evisceration and careful rupture of the gut of a specimen the anterior
end of whose gut had been coloured for more than an hour. The colour dispersed as
the gut was ruptured and the walls were seen to be unstained.
Persistence of colour at the anterior end of the gut presumably implies that the dye
molecules are unable to pass through the gut wall, and the molecular weight of Light
green (793), which is greater than that of amino acids and monosaccharides, bears
this out. Eventual disappearance of the colour seems not to be due to loss from the gut
and therefore presumably indicates the eventual breakdown of the dye molecules.
Complete breakdown is not necessarily implied as loss of colour may ensue from simple
chemical reduction. Different anomopods differ in their ability to break down Light
green. Thus individuals of Daphnia magna that have taken in water containing this
dye via the anus may still exhibit bright green fluid in the anterior portion of the gut
and caeca more than 20 hours later. As in Acantholeberis the source of this colour was
proved by evisceration and rupture of the gut to be the fluid within the lumen and not
stained wall cells. In D. magna and D. longhpina the region which retains colour in
this way extends further back along the gut than is the case in Acantholeberis.
Relevant here is the persistence in the lumen of the anomopod gut of the sometimes
striking coloration (green or golden yellow) often to be seen in suspension feeding
daphnids and bosminids collected in the field. This, as LefGvre (1942) showed for
Daphnia, is derived from pigments released from algal food, and may persist for
several days after the particulate component of the food concerned has been evacuated
from the gut.
That the anterior movement of liquid within the gut involves anal drinking as well
as antiperistalsis can be inferred from the gradual fading and eventual disappearance
of colour posteriorly as the coloured fluid moves anteriorly. Antiperistalsis alone could
produce no more than mixing. Anal drinking other than that which takes place immediately after defaecation has in fact been seen very clearly in Acantholeberis. In an
animal lying ventral surface upwards so that a face view of the anus was obtained, 39
gulps were seen in about 3 min 20 sec before the animal moved off. Defaecation has
been seen in an animal similarly orientated and the ten gulps which rapidly succeeded
each other following this act involved a much wider opening of the rectum than did
this more regular drinking, each gulp of which obviously took in only a little water.
Dilution of the coloured water can also be observed taking place when the animal is
viewed laterally though the muscular movements of the rectum are, from this aspect,
difficult to detect with certainty.
That oral drinking takes place without moving the coloured water posteriorly is
evident, as water must inevitably be taken in with the food. Direct observations of oral
intake of water have also been made. An animal, the anterior end of whose gut was
brightly coloured by a Nigrosin solution taken in largely via the anus, was held in a
266
G. FRYER
compressorium. Such an abnormal situation precludes feeding, but persistent gulping
of water by the oesophagus took place and it is the effectof this intake on the coloured
anterior region of the mid-gut that is relevant here. In 3 min 48 sec, 33 gulps of variable
volume were counted. Especially in the case of the larger gulps a momentary dilution
could be clearly seen as the water was discharged from the oesophagus into the mid-gut.
Although this process continued for much longer than the timed events recorded, the
blue fluid in the gut did not move posteriorly.
In Eurycercus the pattern is similar ; coloured fluids are taken in in relatively small
amounts via the mouth and in larger quantities via the anus, and move forward to the
anterior end of the alimentary canal, being replaced by water posteriorly. Coloured
water taken in via the anus enters the anterior caeca within about 20 minutes or rather
less. As in Acantholeberis this colour persists for several hours though the particulate
gut contents may be replaced several times during this period and much water enters.
SOME IMPLICATIONS OF COPIOUS DRINKING
A puzzling feature of the Anomopoda is the rapidity with which food passes through
the gut. A further, related, problem raised by the observations recorded here is the
effect of the tremendous dilution of the gut contents brought about by the great intake
of water. While this need not seriously affect absorption if much water in fact passes
through the gut walls, dilution of the digestive enzymes is less easy to understand.
The present observations appear to go some way towards rendering these problems
intelligible.
A consequence of the anterior flow of water in the gut would appear to be that much
absorption takes place anteriorly. In the mid-gut of insects there is no doubt that
absorption and secretion can be carried out by the same cells (Wigglesworth, 1953),
and it would not be surprising if this were the case in animals with such an apparently
simple mid-gut as these anomopods. However, there are clear histological differences
between the anterior and posterior gut wall cells in both AcunthoZeberis and Eurycerm.
These are such that one would associate them with anterior secretion and posterior
absorption were it not for the anterior flow of water and conflicting reports concerning
absorption and secretion in the mid-gut of insects. Both histological studies and
experiments on a variety of insects, including the well-studied cockroach, Pertplaneta,
have given such contradictory results (summarized by Wigglesworth, 1953) that one
hesitates to draw conclusions from histology alone, especially when they appear to
conflict with other observations.
In both Acantholeberis and Eurycercus the anterior gut-wall cells are columnar and
are frequently produced into delicate, faintly-staining, villiform or spherical processes
which occasionally appear to break free and lie in the gut lumen. These I would have
assumed to be secretion granules had it not been that Pavlovsky & Zarin (1922, plate 16,
fig. 12) and Henson (1929, plate 5, fig. 11) illustrate what in form and arrangement
appear to be almost identical structures in the mid-gut of the bee, Apis meZl;fera L.
and of the larva of the butterfly, Aglais urticae (L.) respectively, and both offer other
explanations. Pavlovsky & Zarin suggest that these are ‘in most cases artificial’ and
Henson that they are evidence of ‘cell disintegration preparatory to metamorphosis’.
While the latter explanation is obviously inapplicable here, so much controversy
THE CL.4DOCERAN GUT AND DEFAECATION
267
relates to such structures in the mid-gut of insects (Wigglesworth, 1953) that their
nature in anomopods must be regarded as unproven. Certainly, however, they appear
to be confined to the anterior end of the mid-gut in Acantholeberis and Eurycercus and
have been seen in the anterior caeca of the latter. Posteriorly, in both genera, the gut
wall cells are much more flattened.
Observations on the guts of a much wider range of anomopods have revealed further
complexities, and show for example that the distribution of stainable material in the
space between the gut wall and the peritrophic membrane cannot yet be clearly explained. Furthermore, the daphnid gut exhibits less visible differentiation of its
epithelial cells than does that of the macrothricids and chydorids examined. This is so
in representatives of Daphnia, Simocephalus and Scapholeberis. In Moina, usually
regarded as a daphnid but placed in a separate family by Goulden (1968), there is a
similar transition to that seen in Acantholebmk. These differences probably reflect
phylogenetic and ecological (trophic) differences whose significance we cannot at
present assess.
In spite of the superficial cytological similarity of the two ends of the daphnid gut,
the pH is not uniform throughout, being most acidic anteriorly and less so, or even
alkaline, near the posterior end (Rankin, 1929; Hasler, 1935). (How much these
measurements were influenced by the water movements here described is, however,
unknown.) Observations by Rankin (1929) on the transformation of starch to dextrin
in the gut of Simocephalus senulatus (Koch) point to the influence of secretion some
way behind the anterior portion of the mid-gut. Notwithstanding the possibility that
all the mid-gut cells, not only of daphnids but of macrothricids and chydorids, may be
potentially capable both of secretion and absorption, the fact remains that those
located posteriorly must have little opportunity for absorption because of the anterior
flow of water through the gut. This flow, whatever its other functions, inevitably
ensures that such products of digestion as have been derived from the food remain
within the gut and are not voided with the faeces. These presumably include materials
broken down to a stage at which their molecular dimensions are such as to permit
transport by the stream of water but do not allow absorption.
The function of the caeca located at the anterior end of the gut of Eurycercus, all
daphnids, and the macrothricid Ophryoxus has never been satisfactorily explained.
Because of their persistent (but weakly) acidic reaction Rankin (1929) suggested that
they are ‘acidic secretory’ and the histological evidence for Eurycercus would support
this. However, if, as seems inevitable, both enzymes and the products of digestion are
driven forward, then an absorptive role appears highly probable.
It is possible that the cubical cells of the diverticulum of Acantholeberis are absorptive
as there is here no antiperistaltic movement. However, the liquid present in the
diverticulum-originally pure water-is gradually displaced by faecal matter, joins
that at the hind end of the mid-gut, and eventually finds its way to the anterior end.
Furthermore this liquid is continuously diluted by water which enters as a result of
anal drinking. Greater secretory than absorptive efficiency would therefore seem to
be implied, especially as some of the intermediate products of digestion have probably
been flushed from the faeces before they enter the diverticulum.
When particulate food is abundant the mid-gut of daphnids may be packed from
268
G. FRYER
end to end, as it usually is in Acantholeberis. Often, however, the particulate matter is
largely confined to the posterior portion of the mid-gut and the contents of the anterior
portion are for the most part liquid, but usually contain a few fragments of particulate
matter. This liquid is pumped back and forth in the anterior portion of the gut, receives
a steady inflow from behind, and does not itself pass posteriorly. This situation is also
in keeping with the belief that absorption takes place predominantly at the anterior
end of the gut.
Without wishing to revive Putter’s theory, it may be noted that the intake of considerable quantities of water via the gut of these crustaceans provides a feasible
mechanism for the absorption of dissolved organic matter. Some such absorption may
in fact be inevitable. The amounts so obtained are probably small but the possibility
that they are sometimes of significance merits investigation.
It is not claimed that the copious anal intake of water, anterior flow of water within
the gut, and presumed absorption at the anterior end are concerned only with the
prevention of losses of the products of digestion, nor that this is the prime or original
function of anal drinking, but by virtue of such i d o w it would appear probable that
food is utilized more efficiently than would otherwise be the case.
SUMMARY
The posterior loop of the gut of the macrothricid cladoceran Acantholeberis curvirostris, described and illustrated by several authors, does not exist, but a diverticulum is
present. This is associated with a mechanism of defaecation unique within the Macrothricidae, though a similar situation exists in Eurycercus (Chydoridae) and perhaps in
Lgtd9ia. Faecal matter gradually fills the diverticulum, from which it is then ejected
via the rectum. Vigorous anal drinking reflates the diverticulum with water, thereby
restoring body turgor.
Additional water enters the gut via the anus between acts of defaecation and, in
spite of some oral intake, passes to the anterior end of the gut. This implies that the
products of digestion are carried forward and are absorbed, with much water, anteriorly.
Histological evidence of secretion anteriorly is regarded as ambiguous in the light of
conflicting reports concerning insects. In Eurycercus and daphnids water taken in
posteriorly passes anteriorly and enters the caeca, whose functions evidently include
absorption.
Whatever its other functions, anally-swallowed water would appear to prevent loss
of digestion products and to increase the efficiency of food utilization in animals which
may retain food in the gut €or less than 30 minutes.
ADDENDUM
Since the above was written, observations made by Smirnov (1969) on the gut of
certain chydorids, including Eurycercus, have been published. These, which refer to
defaecation and anal drinking, complement those recorded here and also present
quantitative data on food consumption and on rates of peristaltic and antiperistaltic
contractions of the gut.
ACKNOWLEDGEMENT
I am grateful to Miss 0. Forshaw for practical assistance.
THE CLADOCERAN G U T AND DEFAECATION
269
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+
+
ABBREVIATIONS USED I N FIGURES
anus
accessory diverticulum
anterior (muscular) wall of
diverticulum
claw
C
CM constrictor muscles of rectum
diverticulum
D
food filled portion of diverticulum
DF
liquid filled portion of diverticulum
DL
D M dilator muscles of rectum
DSC dark-staining cells
E, E’ endoskeleton and endoskeletal eleme:nts
which support the mid-gut and
diverticulum
A
AD
AW
EC
F
FD
M
MG
MS
NC
PM
PW
R
ss
erroneously supposed course
of the allegedly ‘looped’
gut
fibrils
food/faecal ribbon
delicate membranes in the
ventral space
mid-gut
muscle strand
presumed neurosecretory cells
peritrophic membrane
posterior wall of diverticulum
rectum
sensory seta