The Organization of the Muscular System of
Metridium senile
By E. J. BATHAM AND C. F. A. PANTIN
(From the Zoological Laboratory,
Cambridge)
With two Plates
SUMMARY
I . The muscular system of Metridium consists of fields of relatively short musclefibres. In extension these may exceed i mm. in length but are only about 0-5/* thick.
They can shorten to about a fifth of the extended length. The fibres consist almost
entirely of densely staining material. They form a connected network. At least in some
cases the cells seem to be in contact rather than to form syncytial connexions.
2. Deformation of the body-wall is in part controlled by the contractility of the
muscle-fibres and in part by the properties of the mesogloea. Longitudinal contraction
of the body-wall is accompanied by great thickening of the substance of the mesogloea.
That part of the mesogloea which carries the circular muscle-fibres of the body-wall
does not thicken. It buckles, thereby throwing the muscular layer into folds. Buckling
occurs during the shortening of almost every actinian tissue. The familiar folding seen
in cross-sections of the retractors is a special case of excessive buckling which is
permanent.
3. A natural limit to the extension of anemone tissue is reached when the musclelayer is completely unbuckled. If contraction proceeds to a maximum, there is a
second order of buckling by which the whole body-wall is thrown into folds. Contraction can then proceed no further.
4. The function of the muscle-fields is analysed. The youngest cycles of mesenteries
('imperfect microcnemes') supply the longitudinal musculature of the column (parietal
muscle). The older 'imperfect retractor-bearers' have only feeble parietal musculature,
but possess a retractor muscle connecting the oral with the pedal disk. The perfect
mesenteries have a similar organization to the imperfect retractor-bearers, and particularly in the non-directive perfect mesenteries there is a well-developed sheet of
radial (exocoelic) muscle whose reflex contraction opens the mouth. The vertical
endocoelic muscle-fibres of all non-directive mesenteries fan out on to the pedal disk.
On the exocoelic side, the parieto-basilar fans out from the pedal disk to the body-wall.
As usual, the muscle-fields of the directives are developed on opposite sides from those
of the non-directives.
5. The muscular plan of the pedal disk is compared with the tube foot of Asterias
as described by J. E. Smith. There is a significant functional similarity in the operation of vertical, oblique, and radial muscles (basilars) bearing on the adhesive disk.
The circular layer of the actinian foot has no analogue in the tube foot. It is primarily
concerned with locomotion and not with adhesion.
6. The functional organization of the oral disk and tentacles is discussed. It differs
from the rest of the body in the retention of ectodermal longitudinal muscle. This layer
is responsible for the special movements executed in feeding. The significance of its
physiological separation from the endodermal system is noted.
[Quarterly Journal Microscopical Science, Vol. 92, part 1, March, 1951.]
28
Bathatn and Pantin—Muscular System of Metridium senile
INTRODUCTION
ACTINIANS undergo more extensive changes of shape than almost any
i l other kind of metazoan. The origin and mechanics of their movements
are considered.by us in other papers (Batham and Pantin, 1950a and b). We
shall discuss here the organization of the muscular system by which the movements are brought about in the anemone Metridium senile (L.).
Muscular action in actinians is not simple, and it was necessary at all stages
to compare observations on fixed material with those on living specimens.
Animals were fixed with as little distortion as possible. To avoid distortion
previous anaesthetization is essential. For general anatomical study the
animals selected should be expanded and in good condition. Quiet, darkness,
and exposure for a few hours to a small amount of soluble extract of a mollusc
such as Mytilus help expansion. The best anaesthetic is equal parts of 7^ per
cent. MgCl2.6H2O and sea-water. The expanded animal is left in this solution for one hour or more, during which time the coelenteron is gently and
repeatedly inflated with the anaesthetizing medium. Exposure to menthol
crystals on the surface of the water followed by gentle inflation also provides
good anaesthesia.
Shortly before fixation the animal is transferred to a smaller dish and the
process of inflation continued. A large quantity of the fixative is then run
steadily into the coelenteron. More fixative is immediately used to displace
the 'Mg sea-water' in which the animal is immersed. As fixatives, 5 per cent,
formol, picroformol, Bouin and Heidenhain's Susa were chiefly used. In this
way mesenteries and other tissues could be obtained in such complete expansion that they were on occasion less than 10/x thick. These preparations could
be directly studied as whole mounts under an oil-immersion objective.
Whole mounts and sections 2—8 /u, in thickness were made to trace the musclefibres. Sections were stained with Mallory's triple stain, iron haematoxylin, &c.
The text-figures are taken from, camera lucida drawings or projected images.
In most illustrations the mesogloea is stippled. In tracing the orientation of
muscle-fibres in the muscle-sheets, much help was obtained by direct observation of expanded tissue fixed in 5 per cent, formaldehyde. The direction
of the muscle-fibres could easily be ascertained by stripping narrow ribands
of the muscle-layer from the underlying mesogloea. Carefully done under a
binocular, with the aid of fine forceps, this stripping process gave very clear
pictures of the direction of the muscle-sheets, particularly in the mesenteries
(Text-fig. 3).
The Muscle-cells
The body of a coelenterate consists essentially of a sac of extensible mesogloea upon each surface of which a layer or sheet of muscle-fibres may be
developed. In the actinian the primitive outer muscle-layer is usually absent
over the column, and the inner extends not only round the column but also
over the surface of the mesenteries which project into the gastral cavity.
Batham and Pantin—Muscular System of Metridium senile
29
Change of shape depends primarily upon the contraction of the sheets of
muscle-fibres acting on the fluid in the gastral cavity. Such a system differs
from any we find in other phyla. There is some mechanical parallel with the
condition in Platyhelminthes, where a sub-dermal muscle-layer attached
beneath a basement membrane acts upon a semi-fluid parenchyma. But there
the muscles are developed within the mesenchyme (as they are also in the
Ctenophora) and the semi-fluid system upon which they act is also mesenchymal, and not simply the gastral fluid potentially open to the exterior, a
fact of importance in actinian mechanics (Batham and Pantin, 1950 a).
The more superficial muscle-fibres of actinians retain the primitive condition of uninucleate musculo-epithelial cells (Hertwig and Hertwig, 1879).
In the deeper ones the cell body sinks in and lies alongside the muscle-fibre,
as it does in the mesenteric retractor muscles. The cell body; at least in some
cases, carries a thread-like extension by which it apparently retains its original
connexion with the surface of the epithelium (PL 2, figs, c and d). The musclefibres are unstriated and very thin. PL 1, fig. a, shows the fibres in a typical
section in the plane of the fibres of a mesenteric retractor muscle. Histologically, muscle-fibres from all parts of the body resemble these, except in
size. The extended fibres of the retractor may reach a length of more than
1 mm. The fibre consists of a thin densely staining thread of contractile
material to one side of the middle of which is a mass of less dense protoplasm
containing the nucleus. The dense thread sometimes gives the impression
that it is hollow or that it consists of two halves separated by a narrow core of
less densely staining material. But the diameter of the fibre is so low (0-5 to 1 /x)
that critical determination of structure by ordinary microscopical methods is
not possible. It is, however, certain that almost the whole fibre is occupied by
a densely staining substance, and the apparent high proportion of this to the
sarcoplasm may perhaps be related to the very high tension these fibres appear
to be able to set up (Batham and Pantin, 1950 a).
It was found possible to measure the length of muscle-fibres with ease by
prolonged vital staining with Rongalit-methylene blue (Pantin, 1946). Mesenteries and other tissues were cut from anaesthetized animals. To observe
maximal extension, an anaesthetized mesentery was carefully stretched over
a plate of paraffin wax by means of hedgehog spines. The plate was then
reversed on to a dish of equal parts of sea-water and isotonic MgCl2 containing the stain. We are grateful to Dr. Alexandrowicz for introducing us to this
stretching technique. Times and quantities for optimal staining vary with the
sample of stain. In our work about one drop of stain was added for every
2 c.c. of medium. After some minutes the stain began to be taken up by elements
of the nerve-net. Several hours later individual muscle-fibres also began to
take up the stain. These were easily distinguished from nerve-fibres, which
by that time had become characteristically moniliform (PL I, figs, b and c).
In extended mesenteries the average length of the muscle-fibres was about
o-8 to 0-9 mm. long. In one case a primary mesentery taken from an animal
5-5 cm. high when moderately expanded was stretched under anaesthetic to
30
Batham and Pantin—Muscular System of Metridium senile
6 6 cm. The eight longest vitally stained fibres in this ranged from i-o to
i-8 mm. in length.
The fully extended muscle-fibres are astonishingly thin both in fixed and
in vitally stained material. The apparent diameter even in the mid-region
may be less than 0-5 p. Contracted mesenteries show very greatly shortened
fibres, which naturally are also thicker. Contracted perfect mesenteries, from
the same animal as that giving the extended mesenteries already quoted,
showed fibre lengths ranging from 340/j. to 230^. Next day in dying tissue,
when many fibres appeared to have pulled away from their mesogloeal attachment, the fibres gave the appearance of pencil-like objects, some of which
TEXT-FIG, I . Isometric record of tension developed by ring of circular muscle of column,
2 cm. wide. The preparation was initially suddenly stretched till the tension reached 15 gm.
Note natural maximal contractions and relaxations superimposed on passive extension. Time
in minutes.
ranged from 380 to 170/x long and 2 to 3 ^ in diameter (PI. I, figs, d, e, / ) .
The normal contractions of the body-wall involve shortening to about 25 per
cent, of maximal extension (Batham and Pantin, 1950 a). Free contraction of
individual muscle-fibres exceeds this; they may shorten to 10-20 per cent,
of the extended length.
The great contractility of the muscle-fibres in part accounts for the great
power of the body of actinians to undergo deformation. But this power also
depends on the way the fibres are organized and their relation to the mesogloea
to which they are attached. In thoroughly anaesthetized animals the bodywall can be passively extended to a surprising degree. This passive extensibility implies peculiar mechanical properties in the mesogloea. It raises a
similar problem to the similarly acting basement membranes of animals like
the Platyhelminthes and the Mollusca. The fact that such structures can
exist passively at great differences of extension and yet can provide a firm
basis for the attachment of muscle-fibres is most remarkable. Nor is it the
less so when it is remembered that their staining properties in some ways
resemble those of collagen: a substance not usually distinguished for its
extensibility. There must clearly be some peculiar organization of the fibrous
lattice of such supporting structures to endow them with their observed
mechanical properties. It may also be noted that some at least of the peculiar
Batham and Pantin—Muscular System of Metridium senile
31
so-called 'plastic' properties investigated by Jordan (1934) and by Kipp (1939)
in strips of actinian tissue may in fact not be primarily properties of the
muscles, but of the supporting mesogloea. Text-fig. 1 records an experiment
on a ring about 2 cm. wide which was cut from the body-wall of a Metridium
measuring about 5 cm. across the pedal disk. The ring was set up to record its
tension isometrically. The circular muscle of the ring was at intervals giving
automatic contractions which occasionally were maximal (the three largest
in the record). By stretching the ring, the isometric tension was raised at the
beginning of the experiment. The subsequent changes in tension show first
that the extension of the tissue ring caused by the applied stress proceeds
smoothly and independently of the superimposed natural contractions, and
second that the time scale of muscular relaxation is far briefer than that of
extension of the whole strip. There are evidently two distinct factors operating
during this experiment. We shall shortly recognize two factors operating in
actinian movement: muscular contraction and passive deformation of the
mesogloea.
Organization of the Muscle-fields
Actinian muscle-fibres exceed the maximum length of mammalian plain
muscle-fibres, which reaches 500/i in pregnant mammalian uterus (Maximow
and Bloom, 1948). But they differ from the muscle-fibres of the skeletal
muscles of vertebrates, where a single fibre may extend from the origin to the
insertion of the muscle (Lockhart and Brandt, 1938). More significantly, they
differ from muscles such as the byssus retractor of Mytilus (Fletcher, 1937)
in which also the fibres run from origin to insertion and in so doing may
reach 4-6 cm. in length. This case is the more important because the long
thin unstriated fibres of actinian muscle show some histological similarity to
those of Mytilus.
As Bozler (1941) remarked, there is a functional division between different
kinds of muscle which is more important than the division into striated and
non-striated. He divides muscles into 'multi-unit' types, including vertebrate
skeletal muscles together with such smooth muscles as the cat's nicticating
membrane, and 'visceral smooth muscle' such as mammalian gut, uterus, and
also heart, which consist of a field of muscle-fibres which may behave at least
on occasion as a functional syncytium. The multi-unit types are directly
activated by their motor nerve. The 'visceral smooth muscle' type possesses
the power of automatic activity, and motor activation is more complex and
indirect; particularly, a change in the chemical nature of the medium may
change the response of the muscular field from local activity to contraction
as a single unit. Thus oestrogenic substances cause the mammalian uterus to
pass from a condition of low excitability and local response to one of high
excitability and total response (Bozler, 1948).
'Visceral smooth muscle' is not perhaps the most general designation which
could be applied to this class. Vertebrate cardiac muscle is not smooth; and
among soft-bodied invertebrates, particularly those which are unsegmented,
32
Batham and Pantin—Muscular System of Metridium senile
the dermal and other musculature is 'skeletal' rather than 'visceral' in function, though it may well fall within this class. We prefer to designate the two
classes as 'multi-unit' and 'muscular field' types of organization.
This distinction is important in several ways. The whole muscular system
of Metridium consists of 'muscular fields' in which the fibres, though long
and thin, are in fact very short when compared with the muscles they compose. Even the muscles specialized for a specific function consist of a very
large number of relatively short muscle-fibres.
The fact that these muscles are fields of short fibres implies that the mesogloea and other connective tissue must play a more important part in controlling the mechanical properties of the muscle than in long-fibre muscles
like the byssus retractor of Mytilus. Further, it renders possible either local
activation of part of a muscle-field or its total activation, according to conditions. The fact that muscular activation may be local or total according to
conditions is an essential character of the muscle-fields of Metridium. In this
they agree with 'visceral smooth muscle' of the Vertebrata; they also agree
with this in the very high tendency to inherent activity (Batham and Pantin,
1950J).
Bozler notes that muscles of the 'visceral smooth muscle' class may on
occasion behave physiologically as syncytia, though the morphological
evidence for actual protoplasmic connexion between the fibres is often absent
or equivocal. The fibres of the actinian muscle-fields form an interconnecting
network. They are well seen in preparations of expanded mesenteries showing the sparser muscle-fields outside the region of the retractor (PI. 2). The
fibres appear to be generally unbranched, though short branches may diverge
near their ends. The ends of the fibres commonly run alongside and in contact with adjacent fibres (PI. 2, fig. d). Whether they ultimately make a
syncytial connexion we have not yet determined, but in some cases both with
fixed preparations and after vital staining with methylene blue, connexion
appears to be by contact rather than by evident fusion. In either case these
connected fields offer a potential alternative conducting system to that of the
nerve-net itself. The very slow waves of muscular contraction and peristalsis
seen in the body-wall are conducted at velocities which are to be measured
in cm. per minute rather than in the fractions of a second characteristic of the
nervous impulse.
Anatomy of the Muscular System
A general description of the musculature of actinians has been given by
Hertwig and Hertwig (1879) and by Stephenson (1928). The system of
Metridium marginatum has been described by Parker and Titus (1916).
Examination of M. senile shows that the plan of its musculature is essentially
similar to that of the latter. But for functional analysis these accounts need
amplification and some correction. Text-fig. 2 illustrates the general plan of
the actinian muscle-system and its nomenclature. The system is a hydrostatic one, the muscles working against the volume of fluid in the coelenteron
Bathatn and Pantin—Muscular System of Metridium senile
33
(Batham and Pantin, 1950 a). The body of the animal is roughly divided into
three partially independent functional regions, in each of which the special
muscular system of the body-wall acting against the turgor of the coelenteric
fluid allows the part to take up the shape appropriate to its special activity.
(1) The foot is primarily concerned with adhesion and locomotion. (2) The
capitulum
perfect
non-directive
mesentery
(endocoelic face)
imperFecb
retractor
bearer
(exocoelic face)
parieto
basilar
circular
basilar
One cm.
TEXT-FIG. 2. Illustrating general muscular organization and anatomical nomenclature of
Metridium.
oral disk and tentacle region is primarily concerned with feeding. For this
function it is largely independent of the column. The thin-walled upper pait
of the column, known as the capitulum (Text-fig. 2), should, however, be
included in this region. In Metridium the capitulum acts in concert with the
disk in feeding-reactions and more or less independently of the scapus, or
main part of the column. (3) The most important system governing the shape
of the animal is the musculature associated with the column. In the resting
state this is a cylinder closed at the base by the foot and above by the oral
disk. The oral disk thus plays its part in the column system in addition to its
local functions in feeding.
34
Batham and Pantin—Muscular System of Metridium senile
TEXT-FIG. 3. Photograph of non-directive perfect mesentery of an expanded animal.
Slips of the muscle-fields on both surfaces have been stripped away to reveal direction of
the muscle-fibres. Note (1) the relation of direction to natural stresses in the tissue, (2) the
compensatory relationship of the endocoelic and the exocoelic muscle-fields. The direction
of the outer part of the parieto-basilar muscle-fields is somewhat distorted because anaesthetization has led to unnatural expansion of the base of the column.
Batham and Panttn—Muscular System of Metridium senile
35
It appears to be a general rule in Metridium that the directions of the musclefibres in the muscle-sheets follow the principal lines of stress set up by normal
movements or tonic maintenance of shape (Text-fig. 3). These stresses are by
no means always simply directly vertical or transverse to the axis of the animal.
The so-called transverse or radial muscles of the mesenteries are in fact often
highly oblique (Text-fig. 8c, d). In some cases, however, the stresses run
TEXT-FIG. 4. a. Obliquely vertical section through attachment of a mesentery to the bodywall. Note limited bridges connecting mesenteric mesogloea with that of the body-wall.
The circular muscle-layer (fibres cut transversely) is partly buckled. Note extensive piercing
of mesogloeal connexion by circular muscle-layer, b. Obliquely radial section through pedal
disk and the base of a mesentery. Note firm connexion of mesogloea of mesentery to that
of pedal disk. The circular muscle-field of the pedal disk is cut across radially. Note the
limited channels by which the circular muscle-field pierces the mesenteric-pedal connexion
of the mesogloea.
truly longitudinally and transversely. In both tentacles and column the direction of the muscle-fibres is either along the axis of their cylindrical structure,
or at right angles to it. In the tentacles, for reasons we shall discuss later, the
longitudinal component is supplied by the ectoderm and the transverse by
the endoderm. In the column the endodermal layer of circular fibres provides the transverse part of the system. It is almost continuous round the
body. It passes beneath the mesenteries, the mesogloea of which is only
attached to that of the column at intervals (Text-fig. 4a) (unlike the representation of many text-books). The longitudinal muscle-system of the column
is not supplied by the ectoderm, as in some primitive actinians, but by the
parietal muscles. These are strands of fibres developed along both sides of the
base of the mesenteries, especially in the numerous cycles of the youngest
36
Batham and Pantin—Muscular System of Metridium senile
2 5O>g
TEXT-FIG. 5. Transverse sections of mesenteries showing part of retractor. Muscle-layers
represented by continuous thick line in less magnified drawings. (Actinopharynx on left and
body-wall on right of picture.) a. A fully extended mesentery. Highly magnified portion
of mesentery shown in b as indicated. Note unbuckled general muscle-field (on right), and
permanent external buckling of retractor. Note extreme attenuation of mesogloea. b. The same
extended mesentery under lower magnification, from half-way down column. (Basal diameter
of animal 0-9 mm.) The attenuated mesogloea together with the muscle-layers is represented
by a black line.
c. Very contracted mesentery on same scale as b. (Basal diameter 17 cm.) Note simple
buckling of general muscle-field; and greatly increased thickness of mesogloea, particularly
in the buckled folds of the retractor, d. Moderately contracted mesentery, from level near
pedal disk. The muscle-layer of the retractor showed internal buckling in this specimen.
Batham and Pantin—Muscular System of Metridium senile
37
mesenteries (Text-fig, gb, c). We shall consider them later. The muscular
system of the mesenteries is abruptly discontinuous with that of the column
(Text-figs, ifi and 9).
If both circular and longitudinal systems of the column act synergically
and shorten, water is expelled from the coelenteron. But during most of the
life of the animal these systems act reciprocally. Circular contraction raises
the coelenteric pressure and enforces elongation. Parietal contraction enforces
shortening and widening of the column (Batham and Pantin, 1950 a). The
circular and mesenteric muscle-fields are so extensive and powerful that the
coelenteric pressure must virtually depend on the tone of these alone. Through
the coelenteric pressure they affect the conditions of action of every muscle
in the body.
Buckling, and the Circular Muscle of the Column
The muscular sheet of the column of Metridium consists of a single layer
of muscle-fibres. This lies at the base of the endodermal epithelium in contact with the mesogloea to which the fibres are attached. In the oral disk there
is an additional corresponding sheet at the base of the ectodermal epithelium.
In certain regions special muscles are produced by the repeated folding of
such sheets along the axis of the muscle (Stephenson, 1928). Such folded
muscles are very highly developed in the retractors, where the folds normally
extend out from the mesogloea into the tissue (Text-fig. 5a, b, c). We shall
refer to this as 'external buckling'. Less usually the muscle-layer folds into
the mesogloea (internal buckling) as in Text-fig. $d, a transverse section of a
mesentery low down the column below the level of the ciliated tracts. Textfig. 6b is a vertical section of part of the marginal sphincter. It shows limited
external buckling of the innermost muscle layer which is continuous with the
circular muscle-coat of the column. It also shows the characteristic extreme
internal buckling of the sphincter which in Metridium leads to the pinching
off of ribands of muscle-fibres within the mesogloea. Any actinian shows
some degree of buckling in almost all the muscle-layers if arbitrarily fixed in
a contracted state. Often the folds are neither of the extremes described above,
and will be termed 'simple buckling'.
Buckling plays an essential part in actinian mechanics. The ability of each
element of the actinian muscle-system to shorten is great. As we have already
said, on complete contraction in either direction the body-wall of Metridium
shortens to 25 per cent, of its maximal expansion. This raises the important
question: how does the body-wall accommodate itself to changes in length ?
To elucidate this, sections were cut of animals of various sizes and in various
degrees of expansion. An animal which was fixed in the state assumed during
locomotion (Text-fig, ja) illustrates the influence of degree of expansion on
structure. In such animals the side which happens to be advancing is in a
state of great expansion, whilst the posterior, retreating side is in a state of
contraction. Text-fig, yb, c, and d, show vertical sections through the bodywall of this animal in states of complete expansion, and of moderate and of
38
Batham and Pantin—Muscular System of Metridum senile
greater contraction. At complete expansion the mesogloea is a thin layer to
the inner surface of which is attached a single unfolded layer of circular
muscle-fibres. In the contracted body-wall the epithelia and the mesogloea
have become greatly thickened, apparently in a plastic manner. Round the
column, transversely to its axis, the circular muscle-fibres have of course
shortened. But at right angles to this, in a vertical section of the column as in
Text-fig. 7c and d, contraction has been accommodated in another way; by
throwing the circular muscle-sheet into folds.
TEXT-FIG. 6. a. Portion of vertical section of column showing highly buckled circular
muscle-layer. Note clear, buckled, thin layer of mesogloea to which the circular muscle-fibres
are attached. Muscle-fibres in section seen as black dots. The fibrous detail of the mesogloea
is stylized, b. Vertical section of column in sphincter region showing endoderm, externally
buckled circular muscle-layer, and extremely internally buckled sphincter muscle. In the
latter the folds are nipped off into the mesogloea, only part of which is shown in the figure.
Unlike the greater part of the mesogloea, that part of it in immediate contact with the circular muscle-fibres behaves as though it were a flexible membrane which responded to compression along the axis of the column of the
animal by buckling, and not by becoming shorter and thicker. Thin sections
well stained with Heidenhain's iron haematoxylin show this as a layer paler
than the fibrous mass of the mesogloea (Text-fig. 6a). This mesogloeal
membrane with the attached muscle-fibres constitutes the circular musclelayer. Even when the body-wall contracts greatly with much buckling, the
spacing of the muscle-fibres attached to this layer does not markedly alter.
The effect of buckling on the number of fibres per cm. of body-wall in animals
at different states of expansion is shown in Table I. The first three rows
of measurements were made on the same 4/a-thick sections from which
Text-fig, yb, c, and d were taken. The measurements of the diameter of the
individual muscle-fibres cannot be made with accuracy because their small
Batham and Pantin—Muscular System of Metridium senile
39
cross-section is near the limit of optical resolution. The fibres over most of
their length seem to be fairly constant in size in any one region of the bodywall. A series of estimates was made of the number of fibres which would be
required to span a distance of 5-5p on an eyepiece micrometer. The diameter
was calculated from the mean of several series of five estimates each.
TABLE I
Width of
animal
X height
cm.
I
2
5-2X4-5
3
4
0-9X2-0
5
1-9 X i-o
6
6-SX9-S
Body-wall
Expanded
(Text-fig. 76)
Moderately
contracted
(Text-fig. 7c)
Very
contracted
(Text-fig, yd)
Fully
expanded
Completely
contracted
Moderately
contracted
Length of
circular
ThickmuscleThickness of ness of layer per
body-wall mesogloea cm. of
body-wall
/*
1*
Number
of fibres
per cm.
of bodywall
Number Approx.
of fibres diameter
per cm.
of
of muscle- fibres
layer
M
g,S6o
9,960
05
44
10
I-OI
I3S
40
185
19,150
10,350
o-6
323
62
3-85
37,900
9,940
o-6
coo
o-6
34
225
149
11,300
11,300
66
4-60
35.3OO
7,660
i-o
59
a-94
23.300
7,930
0-7
55
The increase in the number of fibres per cm. of the body-wall owing to
buckling is clear: so also is the comparative constancy of the number of fibres
per cm. across the muscle-layer at different degrees of buckling in the same
animal (column 8).
Numbers 4 and 6 in the table are respectively from a highly inflated small
animal and -a moderately contracted large one. The relation of buckling to
state of contraction seems to be more or less independent of the size of the
animal. Further, the number of circular fibres per cm. of the muscle-layer
(column 8) is less influenced by size of the animal or degree of contraction
than might be supposed.
Number 5 in the table is from a small animal in a state of intense contraction, as in Text-fig, ye. The buckling of the circular muscle-layer is now maximal. But in addition it is accompanied by a second order of buckling, in the
body-wall itself, so that this is thrown into thick ring-like folds (Text-fig. 7/).
The limit is now reached and the body-wall can shorten no further.
At the other extreme, a limit is set to the expansion of an inflated animal
when all the buckled folds of the muscle-layer are smoothed out (Text-fig, yb).
As this state is approached in unpigmented varieties of Metridium, the opaque
White body rather suddenly becomes translucent. Smoothing out of the folds
of the refractile muscle-layer would cause this. Enforced extension beyond this
causes the body-wall to tear irreversibly (cf. Batham and Pantin, 1950 a).
Balham and Pantin—Muscular
50a
ecbodarm
System of Metridium senile
T
mesogloea
muscle endoderm
TEXT-FIG. 7. a. Animal fixed in shape assumed during locomotion. Arrows indicate regions
whence sections b, c, and d were taken, b, c, and d. Vertical sections of body-wall showing
circular muscle-layer unbuckled in complete expansion (6); and in increasing states of contraction, partially buckled (c), and highly buckled id). Note great thickening of mesogloea.
e. Maximally contracted animal, showing in the low-power vertical section (/) the appearance
of buckling of the second order in the whole body-wall.
The limits of extension and contraction of the body-wall are set by the
extension and buckling of the circular muscle-layer; that is, of the superficial
layer of mesogloea to which the muscle-fibres are attached. Similar pheno-;
mena are found in other parts of the muscle-fields except in those where
Batham and Pantin—Muscular System of Metridium senile
41
permanent folding occurs. This temporary folding is an essential feature of
the muscle-sheet of Metridium. The well-known transverse folds of muscles
such as the retractor are in fact simply a permanent expression of the temporary phenomenon seen in the circular muscle-layer of the column. In the
retractors the folds can be exaggerated by further, temporary, buckling, but the
overgrowth of the muscle-layer is so great that they can never be completely
smoothed out by expansion (Text-fig. 5 a).
The existence of temporary buckling warns us to take care when using
folding of muscles as a systematic character. Most fixed actinian material is
distorted and the freely expanded musculature might tell a rather different
story of systematic relationship.
The Mesenteries
Stephenson (1920) showed that in some actinian families such as the
Phelliidae the mesenteries are of two sharply distinct kinds. The microcnemes
are essentially imperfect mesenteries which are little more than a narrow
lamella, possessing no retractor muscle but usually with a well-developed
parietal muscle. The macrocnemes are perfect mesenteries bearing welldeveloped and usually 'circumscript' retractor muscles. In contrast with
these, in families like the Metridiidae the mesenteries seem to show no such
sharp distinction, but to grade into one another.
In M. senile this apparent gradation is somewhat deceptive, and it may well
be so in other cases also. The mesenteries are in fact of three functionally
distinct kinds. (1) The perfect mesenteries extend from the body-wall to the
actinopharynx. Owing to the peculiar mode of asexual reproduction in
Metridium their number varies in different individuals (Parker, 1897). The
directive perfect mesenteries differ in some respects from the non-directives
also. Among the imperfect mesenteries there are two kinds. (2) The imperfect
retractor-bearers closely resemble the perfect mesenteries. They are of some
width and possess a retractor. With the perfect mesenteries they form a
graded series in size. (3) But the numerous mesenteries of the youngest cycles
stand in sharp contrast to the older, the imperfect retractor-bearers, particularly in the absence of the retractor. At this stage they are in fact microcnemes. The difference between the condition in Metridium and that in species
with macrocnemes is that in the former the functional change from microcneme
to retractor-bearer occurs in the youngest cycles, whilst in macrocnemic
species it only occurs with the development of a perfect mesentery.
Imperfect Microcnemes
It will be convenient to describe the mesenteric cycles of a typical example,
which will be that shown in Text-fig. 2. In this, the 9th, 8th, and 7th cycles
of mesenteries were represented only by slight membranes joining the outermost parts of the oral disk to the capitulum. In the 6th cycle there appeared
independently an additional slight membrane between the bottom of the
column and the pedal disk (Text-fig. 8c, j). In the 5th cycle there appears still
42
Batham and Pantin—Muscular System of Metridium senile
another slight membrane below the parapet, joining the sphincter region to
the top of the scapus of the column (Text-fig. 8d, i). In addition, a small ridge
is now developed joining these apparently independent and widely separate
sites of the mesentery's first development. This ridge, which develops from
endocoelic
TEXT-FIG. 8. Mesenteries from specimen in Text-fig. 2. Direction of fibres of muscle-fields
represented by black lines, a-e, exocoelic faces; f-j, endocoelic faces, a and /, perfect
directive mesentery, b and g, perfect non-directive mesentery (cf. Text-fig. 3). c and h,
tertiary, d and i, 5th-cycle mesentery, e and j , 6th cycle. In figures b, c, and / the position
of the retractor muscle on the opposite face is indicated by broken lines, x marks the outer
edge of the pedal disk.
the pedal disk upwards, already possesses a core of mesogloea which bears a
parietal muscle in a relatively highly developed state with marked temporary
external buckling (Text-fig. 9c). This buckling is necessarily most evident in
expanded specimens, where the elongation of the mesogloeal core reduces its
area of cross-section (Text-fig. 96). A comparison of Text-figs. 9c and 96 shows
that, as the anemone contracts, the consequent thickening of the mesogloeal
core somewhat reduces the parietal buckling.
Batham and Pantin—Muscular System of Metridium senile
43
The numerous cycles of microcnemes with their parietal musculature
supply the body-wall with an effective longitudinal muscle-system. Such a
plan has mechanical advantages. We have seen that change in length of the
retracbor
50/*
endocoeli:
50/*
endococlic
TEXT-FIG. 9. Transverse sections through junctions of mesenteries with column wall.
Note in all figures how body-wall circular muscle (here cut longitudinally) almost separates
mesenteric mesogloea from body-wall mesogloea. Cf. Text-fig. 4a. a. Young mesentery of
about 4th cycle. All muscle-layers represented by thick lines. Buckling of parietal muscle
very slight, of retractor strong, b. Young mesentery of about 5th cycle, still only forming
ridge on body-wall. Extremely extended specimen, c. Young mesentery of 5th cycle at halfcolumn level, from moderately expanded specimen shown in Text-figs. 2 and 8. Parietal
muscle in b and c is still highly buckled, and mesenteries have not yet extended inwards to
form sheets of tissue, d. 3rd-cycle mesentery at half-column level, from specimen shown in
Text-figs. 2 and 8. Parietal muscle almost unbuckled.
column is accommodated by buckling of the circular muscle-layer. But if this
same endodermal muscular layer also possessed a continuous sheet of longitudinal muscle there would be difficulty when the column contracted in diameter as well as in length. That would tend to enforce two systems of buckling
at right angles to each other, thereby raising grave mechanical difficulties.
The difficulty is entirely obviated by the arrangement of the longitudinal
44
Batham and Pantin—Muscular System of Metridium senile
muscle in the separate bands of the parietal system. Contraction of the
circular muscle brings the bands closer. The Ceriantharia have apparently
solved the same problem by retaining the primitive ectodermal muscle-sheet,
which is attached to the opposite surface of the mesogloea from the circular
endodermal layer. Buckling of these two layers can thus take place more or
less separately. The actiniarian plan has the advantage in a wide-disked form
since both sets of muscles acting on the disk, the parietals, and the retractors,
are part of the same system. In triploblastic animals these difficulties do not
arise. The dermal muscle-layer of a platyhelminth or nemertine is not based
upon a single layer of muscle-fibres attached to the basement membrane.
Circular, oblique, and longitudinal fibres can all invade the parenchyma
sufficiently to allow free contraction even though they are attached to the
same surface.
The parietal muscle of Metridium mesenteries is derived from two sources.
Most of it comes from the endocoelic face (the retractor side). As we pass
down the parietal, the endocoelic contribution is inserted along the radius of
the pedal disk (Text-fig. 8i). Vertical stress in the column is thus distributed
directly to the pedal disk. On the exocoelic face the small, vertical component
of the parietal gradually fades away as we pass downward. Apparently distinct
from this are the fibres of the parieto-basilar muscle (Text-fig. Sd). These
have their origin towards the centre of the pedal disk and are inserted along
the lower part of the column. The main parts of the two muscle-systems at the
base of the mesentery are thus functionally separate and complementary.
The endocoelic fan transmits vertical stress in the body-wall to the pedal disk;
whilst the exocoelic fan (parieto-basilar) carries any stress which is normal
to the surface of the lower part of the body-wall. Observation and cinematograph films of Metridium suggest that differential contraction of the basal
muscle-fans are important both in bending movements and in locomotion.
When different stresses are taken by muscles of the same field there is an
abrupt change in direction of the muscle-fibres. If on the exocoelic faces of
the mesenteries we follow the line of the parieto-basilar muscle-sheet, the
direction of the fibres changes abruptly as we reach the functionally distinct
parietal muscle.
Passing upwards along the parietal muscle, the endocoelic component
starts to spread inwards just below the parapet (Text-fig. 8z). There is thus
an effective insertion of the parietal muscles on to the marginal sphincter.
It should be noted that this muscle is located on the inner side of the parapet—
thereby marking the upper limit of the main part of the column or scapus.
The sphincter is not situated in the capitulum, which is the tenuous continuation of the column extending from the parapet to the oral disk, as figured by
Parker and Titus (1916) in M. marginatum and diagrammatically by Hyman
(1940). On the exocoelic face a few muscle-fibres run between the inner and
outer sides of the parapet (Text-fig. Sd, e).
When we pass from the main part of the column to the diaphanous capitulum, the microcnemes almost disappear, except for a strand of apparently
Batham and Pantin—Muscular System of Metridium senile
45
endocoelic fibres running out to the edge of the disk. Near the edge, however,
where the mesentery is already developed as a membrane between disk and
capitulum, the endocoelic fibres run outwards to be inserted radially on the
outer part of the disk (Text-fig. 8i,j); whilst the exocoelic fibres directly connect the oral disk with the underlying capitulum (Text-fig. 8d, e). In the
expanded animal, owing to the profound change of shape when we pass from
the main column to the functionally distinct oral disk, we find that the direction
of action of the two muscle-sheets has swung through a right angle. The
endocoelic muscle, which is vertical in the main part of the column, here runs
radially below the outer disk, while it is the exocoelic muscle-layer that pulls
the disk downwards on to the capitulum.
The Imperfect Retractor-bearers
In these the edge of the mesentery has grown radially inwards, thereby
providing a direct connexion between the oral and the pedal disks. This leaves
the mesentery with an arcuate inner edge (Text-fig. 8c, h). The parietal
muscle is now scarcely evident (Text-fig, gd). Through its connexion with the
oral and pedal disks the mesentery can be stretched inward into the gastral
cavity, and when the mesentery is extended in this way the whole of its two
muscle-sheets tends to unbuckle, except for a new muscular element, the
retractor (Text-fig. 9a). When the mesentery becomes rather contracted
radially, and becomes less wide, there is some simple or external temporary
buckling of the muscle-sheets. But the contribution of the muscle-sheets to
the parietal system remains small.
Over a limited region near the free edge, the retractor muscle develops
through the great overgrowth and consequent permanent buckling of the
endocoelic muscle-field (Text-figs. 5 and 9a). Below the middle part of the
column the retractor fans out on to the pedal disk, thereby directly transmitting stress to it from the oral disk. Between the retractor and the column wall
the downward-running fibres of the rest of the endocoelic muscle-sheet are
also inserted radially along the pedal disk (Text-fig. 8/z). When the lower part
of the mesentery narrows and contracts in width radially, this general endocoelic muscle-field is thrown into simple buckling.
As we pass up the mesentery from the mid-region, the fibres of the general
endocoelic muscle-field nearest the column wall fan out on to the parapet and
sphincter. The free edge of the mesentery, however, passes on upwards and
carries the retractor to the oral disk. In so doing, part of the retractor field
swings outwards through a right angle, and running nearly parallel with the surface of the disk fans out upon it up to its edge (Text-fig. 8k). As a consequence
of this, contraction of the retractor pulls the edge of the expanded disk radially
inwards, before it is engulfed downwards within the closing marginal sphincter.
Just below the parapet, and between the parapet and the column, the imperfect retractor-bearing mesentery develops a 'marginal stoma'.
Most of the exocoelic musculature is weak, except for the parieto-basilars
which are like those of the microcnemes. They are sufficiently developed to
46
Batham and Pantin—Muscular System of Metridium senile
undergo simple buckling when the mesentery contracts radially (Text-fig. 1 ib).
Above, there are a few fibres running obliquely upwards from the upper part
of the scapus to the free edge of the mesentery. Still farther above, a sheet of
fibres connects the capitulum with the oral disk. In the mid-region there are
a very few exocoelic fibres which run obliquely upwards. Nearer the free edge
there are no evident exocoelic fibres till we approach the mesenterial filament.
This intensely active and largely independent structure is supported by a
local development of muscle-fibres.
The retractor muscles are far stronger than is needed simply for the
maintenance of tonic form. They serve two functions. Their slow tonic contraction plays its part in maintaining the shape of the column in concert with
the parietals. But on sudden stimulation their rapid contraction leads to
shortening and closure of the anemone. In the fast retraction response the
powerful retractor muscles of the mesentery act antagonistically through the
fluid of the coelenteron not only to the circular muscle of the column but also
to some extent to the parietal musculature. Their sudden contraction leads
to a withdrawal of the disk which may cause a general bulging outwards of
the whole body-wall. This retraction is accompanied by contraction of the
radial musculature of the disk and is immediately followed by contraction of
the well-developed sphincter muscle which covers it. The retractors and the
sphincter may be termed specific effectors. In addition to the minor part they
play in concert with the rest of the muscle-fields in the maintenance of tonic
form, their sudden contraction directly leads to a special response, to execute
which they must be much more powerfully developed than the general musclefield. We shall see other examples of specific effectors.
The Perfect Mesenteries
Except that these extend right across to the actino-pharynx, the perfect
mesenteries are functionally similar to the imperfect retractor-bearers (Textfig. 8a, b,f, g). They possess one new feature of importance. In all the perfect
mesenteries there is a sheet of radially running muscle-fibres inserted on the
wall of the actinopharynx. In the non-directives the sheet is exocoelic on
the face opposite the retractors. This radial sheet is rather less evident in the
narrower, directive mesenteries, where the (here exocoelic) retractor lies close
up to the siphonoglyph (Text-fig. 8a).
The contraction of these radial muscles, particularly in the non-directives,
opens the actinopharynx by pulling it outwards and laterally. Collectively
they constitute an important specific effector. Their 'reflex' contraction permits controlled loss of fluid from the coelenteron (Batham and Pantin, 1950 a).
Their action is also clearly seen in quick-motion pictures, and by direct
observation during the ingestion of solid food. The contraction of the muscles
causes vertical lines to appear at five or six places in the body-wall. These
lines correspond to the insertion of pairs of perfect mesenteries.
The perfect mesenteries possess an additional stoma, the oral, piercing the
mesentery between the disk and the actinopharynx (Text-fig. 3). The oral and
Batham and Pantin—Muscular System of Metridium senile
47
marginal stomata are weakly sphinctered and their size can be varied. They
are manifestly important in a system filled with fluid and subject to extensive
movement.
We have now completed our survey of the numerous cycles of mesenteries
by which the coelenteric pressure on the oral disk is transmitted to the column
and pedal disk. The well-arranged pattern of the radial mesenteric insertions
ensures that no point on the disk is more than a few mm. from some underlying tie. In contrast, the column wall with a radius of 50-60 mm. must have
strength to withstand much higher relative tensions in its substance to take
the stress set up by the coelenteric pressure. Consequently the disk can remain
thin walled in comparison with the column. The actiniarian plan of mesenteric
cycles is peculiarly well fitted to support a wide but thin-walled and labile
disk. It may be that the success of this group in producing wide-disked forms
is attributable to this feature. The condition in the Ceriantharia where the
mesenteries are weak and imperfectly radially symmetrical, and where the
primitive longitudinal muscle-system of the ectoderm is retained, may be
contrasted with it.
The Pedal Disk
The endoderm of the pedal disk carries a sheet of concentrically arranged
circular muscle-fibres (Text-fig. 4^) continuous with the circular musclelayer of the column. Unlike the oral disk the ectoderm has no evident musculature of its own. Its cells, however, possess a very marked fibrous structure.
These fibres are firmly fixed to the mesogloea and run down to the lower ectodermal surface (Text-fig. 10). Though arising from the mesogloeal surface,
the ectodermal fibrils are quite different from mesogloeal fibres. In Mallory's
triple stain the latter colour strongly with aniline blue, whereas the ectodermal
fibres stain with acid fuchsin. In this and in their affinity for iron haematoxylin
the ectodermal fibres resemble muscle-fibres, notwithstanding their orientation transverse to the ectodermal epithelium. They differ from muscle-fibres
in several particulars. First, they are considerably finer even than the thin
extended -muscle-fibres. Secondly, they seem to be formed between the
elongated ectodermal cells rather than intracellularly. Thirdly, sections of
expanded pedal disk seem to show the fibrils irregularly folded, rather than
shorter and thicker, as they would be if they were contractile. Nevertheless, the
possibility that the fibres are on occasion contractile cannot be ruled out.
In specimens of Metridium that have been attached for a little time the pedal
disk surface secretes on to the substratum a cuticle, as shown in the figure.
The ectodermal fibres thus provide a firm temporary connexion between the
mesogloea and the substratum. Other organisms resort to devices convergent
with this method of attachment where it is necessary to transmit strain through
an epithelium to the substratum. Smith (1947) has shown in the tube-feet
of Asterias the manner in which strands of connective tissue extend through
the ectoderm of the adhesive disk. In the giant species of Myriothela, which
presents some interesting convergences with actinians, the mesogloea itself
48
Batham and Pantin—Muscular System of Metridium senile
makes direct contact with the substratum at places of attachment (Manton,
1940).
The mesenteries are firmly attached to the pedal disk by the mesogloea.
The base of the mesenteric mesogloea is pierced by tubes carrying circular
muscle of the disk, but the attachment is stronger and far less interrupted in
this way than is that between the mesentery and the wall of the column (cf.
Text-fig. 4a and b).
mesogloea
25/*.
TEXT-FIG. 10. Section through pedal ectoderm with adjacent mesogloea. Note temporary
cuticle (left) by which pedal disk is attached. Note ectodermal fibrils running between cuticle
and mesogloea. Note complexity of structure of the mesogloea.
The only intrinsic muscle of the pedal disk is the sheet of circular fibres.
Radial fibres are, however, supplied by the basilar muscles of the mesenteries.
The basilars (Text-fig. n a ) are strands of muscle with permanent external
buckling. They run on one or both sides of the attachment of the mesentery
to the pedal disk. Collectively they form a powerful system. In interpreting
the manner in which the pedal disk functions, the parieto-basilars and the
lower fans of the retractors and other endocoelicfibresmust be also considered.
The foot has two main functions: adhesion and locomotion. Let us first
consider adhesion. There is a striking parallel between the functional organization of the pedal musculature of Metridium and that of the tube-foot of
Asterias as described by Smith (1947). In both there is longitudinal muscle
running up the wall of the column, and also muscle-fibres running obliquely
from the walls towards the centre of the attachment disk. These are the
exocoelic fans and the parieto-basilars in the actinian, the levator muscles in
the tube-foot. In both cases there is a well-developed radial musculature.
Bathatn and Pantin—Muscular System of Metridium senile
49
As Smith points out, the levator and the radial muscle-systems of the tubefoot supply the sufficient muscular apparatus for adhesion; tension in the
levator tends to raise the centre of the adhesive disk, thereby causing suction
between the disk and the substratum. Conversely, contraction of the radial
muscles tends to raise the pressure beneath the disk and thereby facilitates
release.
exocoelic
eiocoelic
TEXT-FIG, I I . a. Vertical tangential section through pedal disk and the base of a contracted
retractor bearer. Note well-developed and permanently buckled basilar muscle-tongues on each
side of attachment of mesentery to pedal disk. Note circular muscle-fibres of pedal disk cut
tangentially, and absence of ectodeimal musculature (below), b. Vertical tangential section
through pedal disk and a contracted retractor bearer. Note the buckled parieto-basilar musclefield along the upper exocoelic surface of the mesentery. It is distinct from the basilar elements
below.
In Metridium tonus is present in the parieto-basilars and in the basal
endocoelic muscle-fans in order to oppose the coelenteric pressure. The consequent tension in these muscle-fields must necessarily tend to promote
adhesion, as in the tube-foot. Their action may be seen in the inward arching
of the pedal disk when an anemone is removed from its hold on the substratum.
Under appropriate conditions contraction of the radial musculature, the
basilars, may well facilitate release of the foot just as in the tube-foot, especially if accompanied by the secretion of mucus. It is noteworthy that in the
reverse process, that of attachment to the substratum, Metridium first expands
the foot through relaxation of the radial musculature. But the release of the
extensive and mobile pedal disk of an actinian presents a more complex problem than that of a tube-foot, especially when attached to an irregular or concave
surface. And while release is a regular element in the mechanical operation of
a tube-foot, it is a comparatively rare phenomenon in an actinian. Occasionally
Metridium will release its hold spontaneously and fall to the bottom of the
50
Batham and Pantin—Muscular System of Metridium senile
aquarium; but commonly there are only two alternative states, adhesion and
locomotion.
Besides the similarities there are some interesting differences between the
actinian and tube-foot systams. The tube-foot disk has a powerful supporting
ring of connective tissue, while the mesogloea of the foot of Metridium is
necessarily thin and extensible. This may be connected with the differentiation
of the 'levator' system in Metridium into two complementary parts, the
endocoelic fan and the parieto-basilars. These latter, acting upon the flattened
pediment of the column and the contained coelenteric fluid, give the edge of
the foot considerable rigidity, as can be seen in detached specimens. They
thus confer on the pedal disk some of the advantage of the rigidity enjoyed
by the tube-foot by virtue oi its connective-tissue ring.
The most striking difference between the adhesive disk of the tube-foot
and the pedal.disk of Metridium is the presence in the latter of the circular
muscle-layer. Tension in this must necessarily influence the pressure below
the pedal disk which determines adhesion or release. But we see from its
absence in the tube-foot that such a layer is not a necessity for an adhesion
mechanism. Both the radial and circular musculature of the foot of Metridium
are concerned with another and important function, locomotion. During this
complex process waves of contractions involve the whole of the musculature
of the pedal disk: we shall discuss this in a later paper.
The Tentacles and the Oral Disk
The muscular organization of the disk differs from that of the column.
The mesenteries do not contribute important radial muscles to the oral disk
comparable to the basilars of the pedal disk. Unlike the column, in both
tentacles and disk there are muscle-sheets on each side of the mesogloea.
There is an endodermal circular layer corresponding to that of the column,
but the radial musculature is supplied by the ectoderm. Each can contract
independently. Contraction causes mesogloeal thickening, and both musclelayers of the disk and of the tentacles can undergo simple buckling. The two
lavers can do this simultaneously because they are on opposite sides of the
mesogloea (Text-fig. 12).
The possession of the primitive ectodermal longitudinal muscle-system in
the tentacles and disk is morphologically a fundamental difference from the
condition in the column. The radial and longitudinal muscles of the disk and
tentacles are important direct effectors for a specific reaction—feeding. The
whole complex sequence of food capture leading to ingestion in actinians
(Pantin and Pantin, 1943) involves bending of the tentacles by local contraction of their longitudinal muscles. Thus the localized responses of food
capture are effected by a muscular system which, being ectodermal, is distinct
from the main endodermal muscular system controlling form. It is this same
ectodermal system of the disk and tentacles that shows the most striking local
neuromuscular action, accompanied by interneural facilitation and independence of the column system (Pantin, 1935).
Batham and Pantin—Muscular System of Metridium senile
ectoderm
ect.
\J
51
Lmus. circ. muscle
I mes] endoderm
circ. muscle,
mes. I en.
u
e »-•
G. ia. a-d. Sections of Metridium tentacles. Mesogloea is left unstippled. a and
b. Transverse to tentacular axis: a extended; b contracted. Note simple buckling of ectodermal
(longitudinal) muscle-field, c and d. longitudinal sections: c extended; d contracted^ Note
relative -weakness of circular muscle-field, and simple buckling on contraction, a and c are
from the same tentacle from one of the outer cycles. (Pedal diameter of animal S'i cm.)
b and d are from the same tentacle from the innermost cycle. (Pedal diameter a-a cm.)
e. Longitudinal section of extended body-wall on same scale. Compare this more uniform
and compact muscle-layer with tentacle musculature.
cmc, circular muscle; EN.endoderm; ECT, ectoderm; M, MES, mesogloea; L.MUS, longitudinal
muscle.
52
Batham and Pantin—Muscular System of Metridium senile
The ectodermal position of the longitudinal muscle-fibres of the tentacles
is also of mechanical significance. As in Hydra and other coelenterates,
in this situation the longitudinal fibres can exert a great bending moment
on the tentacle. They could not do so as effectively if they were attached
to the inner surface of the mesogloea, with the circular fibres on the outside.
Not only would the lesser distance of the fibres from the tentacular axis
reduce the moment flexing the tentacle, but the resistance of the mesogloea,
now outside the contracting fibre, would actually oppose this flexion.
The longitudinal and the circular systems of the tentacles have very different
functions. The muscle-fibres of the former are much stronger and more
numerous than those of the, latter (Text-fig. 12). The longitudinal fibres are
important specific effectors, and their contraction must be powerful enough
to enable the tentacles to transport food objects of considerable size to the
mouth. On the other hand, the circular muscle-fibres are primarily concerned
with tonic maintenance of shape, and because of the low coelenteric pressure
and the small diameter of the tentacles compared with that of the column, a
feeble muscularity suffices. This follows because, like the column, the tentacle
of an anemone is essentially a cylinder. At any particular internal pressure,
the tension set up in the walls is proportional to its radius. Consequently a
given internal pressure which demands a certain strength of muscle and toughness of the mesogloea in the wide column will require much thinner structures
in the narrow tentacles. In agreement with this we find that when the tentacle
is fully expanded the mesogloea is much thinner and the circular musclefibres somewhat fewer and more irregularly spaced than in the column (cf.
Text-fig. 12c and e).
In spite of their weaker development, the circular muscle-layers of the
tentacles are part of the same endodermal tonic system as that of the endodermal muscles of the column. Because of their small size and volume, contraction of the tentacles has little effect on the general form of the body
through changes in coelenteric pressure. This contrasts with the great effect
of the powerful muscle-fields of the column. But the tonic function of the
circular muscle of the tentacles is of great local importance in the tentacles
themselves. The tentacles of actinians are capable of considerable extension
in length. This is possible because of their hollow structure and the highly
extensible character of the mesogloea. But coelenteric pressures which suffice
to cause extension of a hollow tubular tentacle must be met by some circular
tension elements able to resist the tendency of the wall to bulge outwards.
Smith (1947) has shown that in the tube-feet of Asterias this same mechanical
problem is met by an ingenious device; the presence of a layer of inextensible
supporting rings of connective tissue in the wall of the foot. There is no such
device in the tentacles of Metridium, and here the transverse tension must be
met by contractile elements, the circular fibres. The great tentacular extensibility and the presence of circular muscle-fibres suggest a similar mechanism
in the tentacles of Hydra; but we know nothing yet of the coelenteric pressure
in the Hydras.
Batham and Pantin—Muscular System of Metridium senile
53
If great extension in length is not required by a tentaculate organism, a
circular muscle-layer is no longer necessary. The endoderm can then be converted into a solid but flexible rod which is bent back and forth by the longitudinal muscle-fibres of the ectoderm. This condition is often found in
hydrozoan polyps, including those of Obelia. The endoderm becomes a rod
of vacuolated cells resembling the notochord cells of Chordata (Fowler, 1900).
The longitudinal muscle-fibres of the ectoderm may now suffice for any
necessary tentacular movement; just as longitudinal fibres alone suffice in
other animals with more or less inextensible tentacles, as in Sabella pavonina
and many ectoproct Polyzoa. In the majority of Hydrozoan polyps we have
in fact a different principle of tentacular skeletal action from that of Metridium.
This new principle of direct action of muscle against a flexible solid skeleton
is extensively employed among coelenterates, as in the bell of medusae of all
kinds. It may also play some part in actinian mechanics where the mesogloea
is thick and tough, like that of Calliactis parasitica.
. Perhaps the most interesting feature of the muscular system of Metridium
is the contrast which it presents to that of a more highly organized animal,
such as an arthropod or a vertebrate. In the latter the somatic musculature
is organized as well-defined muscles developed to meet specific functional
needs. In the actinian there are a few similarly differentiated specific effectors,
like the retractor and the marginal sphincter. But most of the musculature
consists of more or less undifferentiated sheets of muscle covering the bodywall and its extensions, the mesenteries. As we have shown elsewhere (Batham
and Pantin, 1950 a), contraction of these muscle-sheets has complex indirect
as well as direct effects on the shape of the animal. A particular movement of
the body necessarily involves a complex pattern of contraction and extension
in the various muscle-sheets of the animal's body-wall. Simplicity of muscular
action is onjy attained through the development of specific effectors, like the
retractors. Their simplicity of mechanical action and the simplicity of the reflex mechanism of their activation via the through-conduction system (Pantin,
1935) are secondary simplifications to meet specific environmental needs.
We thus arrive at a curious paradox. Physiologically the simplest parts of
the neuromuscular system are in fact the most specialized; whilst the less
differentiated parts, the muscle-sheets, inevitably require complex differential
co-ordination if their contractility is to be translated into effective movement
of the body (cf. Batham and Pantin, 1950 b). Such complex co-ordination has
often been treated as a product of the more advanced stages of neuromuscular
evolution; but it must of necessity be present in some degree in the least
differentiated organisms. It must be present in them for the very reason that
they lack differentiated effectors, the action of which could simply and directly
meet their functional needs.
Much of this work was done at the Marine Biological Laboratory, Plymouth,
and at the Stazione Zoologica at Naples, to the Directors and staffs of which
54
Bathatn and Pantin—Muscular System of Metridium senile
we are most grateful for the many facilities given us. Part of the work was done
during the tenure by one of us (E. J. B.) of a Shirtcliffe Fellowship of the
University of New Zealand. We also wish to thank the Department of
Scientific and Industrial Research for a grant for the development of a special
research which enabled this work to be concluded.
REFERENCES
BATHAM, E. J., and PANTIN, C. F. A., 1950a. J. exp. Biol., 27, 264.
19506. Ibid., 27, 290.
BOZLER, E., 1941. Biol. Symp., 3, 95.
1948. Experientia, 4, 213.
FLETCHER, C. M., 1937. J- Physiol., 90, 233 and 415, and 91, 172.
FOWLER, G. H., 1900. A Treatise on Zoology. Ed. by E. Ray Lankester. Part II. London
(Adam & Black).
HERTWIG, O., and HERTWIG, R., 1879. Jena. Z. Naturw., 13, 457.
HYMAN, L. H., 1940. The Invertebrates: Protozoa through Ctenophora. New York and
London (McGraw Hill Book Co.).
JORDAN, H. J., 1934. Arch. nee>l. Physiol., 1, 1.
KIPP, P. J., 1939. Ibid., 24, 426.
LOCKHARDT, R. D., and BRANDT, W., 1938.
J. Anat., 72,
470.
MANTON, S. M., 1940. Brit. Graham Land Expedition Sci. Reports, 1, 255.
MAXIMOW, A. A., and BLOOM, W., 1948. Textbook of Histology, 5th ed. London (W. B.
Saunders Co.).
PANTIN, C. F. A., 1935. J. exp. Biol., 12, 119, 139, 156.
1946- Notes on Microscopical Technique for Zoologists. Cambridge (University Press).
and PANTIN, A. M. P., 1943. J. exp. Biol., 20, 6.
PARKER, G. H., 1897. Bull. Mus. Comp. Zool. Harvard, 30, 259.
and TITUS, E. G., 1916. J. exp. Zool., 21, 433.
SMITH, J. E., 1947. Quart. J. micr. Sci., 88, 1.
STEPHENSON, T. A., 1920. Ibid. 20, 419.
1928. The British Sea Anemones, vol. 1. London (Ray Society).
EXPLANATION OF PLATES
PLATE I
(a) Vertical (ion) section of retractor showing muscle-fibres. Fixed in Susa; Mallory's
triple stain.
(6) and (c) Well extended muscle-fibres of vertical muscle-fields of retractor, vitally stained
with Rongalit-methylene blue. Note also over-stained fibres of nerve-net undergoing moniliform degeneration.
(d), (e), and (/) Similarly vitally stained retractor muscle-fibres after undergoing maximal
contraction.
Figs. (6) to (/) are on the same scale.
PLATE 2
Weak vertical muscle-field on endocoelic face of highly expanded perfect mesentery, between retractor and body-wall.
(a) Drawing to show connexions of fibres in part of muscle-field shown in (c).
(A) Drawing to show cell bodies and processes running to epithelial surface. From part of
muscle-field adjacent to (c).
(c) Preparation fixed in picro-formol and stained with iron haematoxylin. The epithelium
has been partly brushed away to expose the muscle-fibres more clearly.
(d) Highly magnified portion of muscle-field showing a cell body (above X), and a junction
between two muscle-fibres (above V).
Quart. Journ. Micr. Sci. Third Series, Vol. g2
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E. J. BATHAM & C. F. A. PANTIN—PLATE I
Quart. Journ. Micr. Sci. Third Series, Vol. 92
II
I
25>u
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E. J. BATHAM & C. F. A. PANTIN—PLATE II
Y