AMER. ZOOL., 14:719-734 (1974).
On the Mechanics of Growth and Morphogenesis in Hydroid Polyps
L. V. BELOUSSOV AND J. G.
DORFMAN
Department of Embryology, Moscow University, Moscow 117234, USSR
SYNOPSIS. The growth and morphogenesis of Obelia loveni and Dynamena pumila
asexual generation were studied. Their cell layers consist of tightly packed cells which
are able to contract, to icorient and slide upon one another while remaining at the
same time anchored to elastic enveloping membranes. Both growth and morphogenesis
are of pulsatory character due to coordinated periodic contractions and relaxations of
cells. Cell contraction results in a normalization of cell orientations, an upward shift
of the entodermal column, and an expansion of the rudiment's tip. Cell relaxation
is accompanied by reverse deformations and an upwards shift of the ectodermal column. The spatial pattern of active and passive forces and supporting structures is
ascertained.
Morphogenetic processes in hydroids are demonstrated to be the results of some
natural modes of behavior of tightly packed contractile cells integrated into a single
mechanical system.
A description o£ a developmental process
may be regarded as really valuable if it
not only reflects in detail the observed
phenomena, but, in addition, reduces to
a manageable extent the number of independent variables characterizing a developing system. In applying this principle to
pure morphogenetic processes, e.g., to the
process of geometric alterations during
development, the aim of a satisfactory description would be to avoid the necessity
of introducing a new independent morphogenetic factor for each more-or-less pronounced local alteration of shape and/or
of direction of growth. Not only the general reasons of minimization and scientific
elegance, but the far more concrete task
of overcoming the well-known preformistic
deadlocks, demand that an initial organization of a rudiment be in no way so
complicated as to contain in itself each
morphological difference of a developed organism. In this report, an attempt is made
to give such a "minimized," "non-mosaical"
description of some morphogenetic processes in hydroids.
The authors are greatly indebted to Drs. L. A.
Badenko, A. L. Katchurin, G. G. Petrov, and B. G.
Safronov for their valuable assistance in time-lapse
filming, and to Dr. C. R. Wyttenbach for many
comments which helped to clarify the English text.
This description, for several reasons, may
be designated as "mechanical." First, insofar as morphogenesis in its strict meaning
is a mechanical process (a process of movements of some material units), we believe
it cannot be satisfactorily described without pointing out the sources of active and
passive forces, the supporting structures,
and other purely mechanical aspects. Moreover, the general conditions of mechanical
equilibrium are clearly valid for the great
majority of developing rudiments. This
leads to a considerable reduction in the
number of possible geometrical patterns
and their transformations.
Two species of marine hydroids (Thecaphora)—Obelia loveni and Dynamena
pumila (the same as the North American
Gonothyraea loveni and Sertularia pumila)
—were the main objects of the study. The
methods employed were much the same
as those described in Beloussov et al., 1972.
In that paper, the development of the
asexual generation of both species was described. The detailed and precise character of the morphogenesis during rudiment development was evident (see Figs.
1, 2 in Beloussov et al., 1972). A number
of experiments and observations demonstrated cell movements, rather than proIiferativc processes, to be the direct basis
of rudiment growth and morphogenesis.
719
720
L. V. BELOUSSOV AND J. G. DORFMAN
of the basal membrane. This is the most
effective contractile system of the Hydrozoa. However, it seems that no myofibrils
exist in the tip regions of growing rudiments, i.e., in the areas of the most active
morphogenesis (Hale, 1960). They appear
only at some distance below the tip, in the
so-called "contractile zone," and are particularly well developed in adult hydranths.
Entodermal cells seem to be closely fixed
at the corresponding lamina of the basal
membrane. Ectodermal cells can shift to
some extent towards and away from the
basal membrane, keeping (at least in the
majority of cases), however, filamentous
contacts with it. Similar, but perhaps firmer
contacts, allowing only small normal shifts,
THE STRUCTURE OF HYDROID EPITHELIA
exist between these cells and the common
surface (obviously elastic) membrane of
The character and mechanisms of cellu- the ectoderm, which may be called a "plaslar movements in hydroids largely depend malemma." The latter is to be distinguished
upon the structure of their epithelia. The from the hydrotheca or perisarc, the chibody of a hydroid (usually designated as tinous layer which is built up at the excoenosarc) consists of two layers (ectoderm ternal surface of the plasmalemma in the
and entoderm), between which there are tip region.
no stable mechanical junctions. The basal
The newly laid hydrotheca of tip regions
membrane separating the layers consists of
two laminae, to one of which are fastened is fairly soft and does not prevent expanentodermal and to the other ectodermal sion of the growing rudiment. In all healthy
cells. The layers are capable of mutual rudiments the plasmalemma of the tip
normal and tangential shifts. Both consist regions is closely fitted to the hydrotheca,
mainly of myoepithelial cells. Those of which, however, in no way prevents the
the entoderm are much like common epi- tangential shifting of the plasmalemma.
thelia, whereas those of the ectoderm are Perisarc of slightly more proximal regions
spindle or barrel shaped and have a fibril- is already completely rigid. It remains fixed
lar structure. Areas of close contact be- even after the contraction of the corretween the neighboring cells occupy only sponding area of coenosarc (e.g., during
small parts of the lateral cell walls and are the formation of the hydranth "neck").
localized in parabasal regions of the ento- Already the structural organization of the
dermal layer and along the midline of the tissue layers of hydroids as here described
ectodermal layer. Fibrillar structures of the leads to the conclusion that some of their
ectodermal cells (the so-called tonofibrils) elements (individual cells) are active,
seem to play not only a supporting (as whereas others (hydrotheca and plasolder authors believed) but also a con- malemma) are passive. The latter structractile role, being able to alter cell shape tures will be demonstrated to play a role
(Hale, 1960). Our own evidence in this which both supports the rudiment shape
respect will be presented in what follows. and accumulates mechanical energy.
The following set of facts provides addiBesides this type of contractile structure
which is oriented along the cell axes, there tional information about the characteristics
exists a net of myofibrils, composed of of the passive and active elements:
fibrillar outgrowths of both ecto- and
1) After incomplete inhibition of the
entodermal cells, and situated in the plane metabolism of developing rudiments, a
The areas of cell proliferation do not, as
a rule, coincide with those of active morphogenesis (in the studied species, particularly, the first are located near the stem
bases, whereas the latter are at the tips of
the rudiments), and there is no direct
correlation between concentration and
orientation of dividing cells and the shape
and growth of a rudiment (Beloussov,
1961, 1963; Crowell et al., 1965; Campbell,
1967; Webster and Hamilton, 1972). At
the same time, the establishing of a certain cell density seems to be the necessary
prerequisite for morphogenesis (e.g., Webster and Hamilton, 1972).
MECHANICS OF HYDROID MORPHOGENESIS
partial reversion of their morphogenesis
takes place, i.e., a rudiment returns to its
previous, more rounded shape (see details
in Beloussov et al., 1972). One may suppose that this is due to the action of elastic
"smoothing" forces of the passive enveloping membranes, which overcome under
such conditions the inhibited shaping activities of the myoepithelial cells.
2) The orientation of cells in actively
developing l udiments is as a rule perpendicular (normal) not to the present but
to the future contour of the rudiment
(Beloussov, 1967; see Figs. 10, 14 in Beloussov et al., 1972). This kind of cell orientation, which is the earliest indication of the
direction of subsequent growth and/or
shaping of the rudiment, may be designated as "prognostical."1
The following experiments demonstrate
that the prognostical character of cell
orientation is not a mere coincidence, and
points out some real causal relations. As
mentioned in Beloussov et al. (1972), the
direction of growth of each of three adjacent rudiments in D. pumila (one so-called
central rudiment—CR, and two symmetrical lateral rudiments—LR's; Fig. \A) depends upon the presence of its neighbors.
If the CR is removed, each of the LR's,
instead of bending sideways, grows approximately vertically (Fig. \B,C). ]f one of the
LR's is removed, the CR inclines towards
the space left (Fig. ID). These alterations
in growth directions are preceded by regular cell reorientations in the walls adjacent to the removed rudiment. Thus, the
cells of a CR wall adjacent to a removed
LR become orientated more perpendicularly to the outer surface of the rudiment
than in the opposite wall (see Fig. l\B in
Beloussov et al., 1972). Cell orientation in
the CR as a whole becomes asymmetrical,
"predicting" a subsequent turning of the
CR towards a removed LR in the same way
as an asymmetrical cell orientation in an
Obelia stem "predicts" its eventual turn1
The phenomenon of "prognostical" cell orientation was first described by Gurwitsch (1914) in
developing neural rudiments of vertebrate embryos.
721
ing away from the maternal stem (cf. Figs.
10/4,5 and IIB in Beloussov et al., 1972).
In both cases the rate of elongation of a
wall with the more perpendicular cell
orientation is slower than the opposite one,
leading to subsequent bending of the
rudiment.
It should be mentioned that the normalization of cell orientation in a CR wall
takes place not only after complete removal
of the LR, but also after a breaking of
structural contacts between the CR and the
LR by simple cutting or by insertion of
a celloidin membrane between them (Fig.
\E,F). The LR, separated by a membrane
from the CR, grows more vertically than
normal (Fig. 1£). Thus, the effect of
breaking structural contacts between the
rudiments seems to be identical to that of
their removal. It should be emphasized as
well that the first signs of cell normalization in the CR ectoderm become visible
within a few minutes after the removal of
the LR or its dissection from the CR (Fig.
IF and the following section).
3) If an as yet smooth ectodermal "roof"
of a D. pumila CR is separated from the
underlying entoderm by dissection (Figs.
\G, 2/4) or, in addition, from the basal
parts of the ectoderm itself (containing the
myofibrils, Fig. 2B), it rapidly folds (in
2 to 3 min after separation), imitating the
typical morphological differentiation of a
CR (namely, its subdivision into three
rudiments by two deep grooves). The first
conclusion obtained from these results is
that the parabasal myofibrils, even if really
present in the distal parts of the rudiments
(remember Hale, I960, cited earlier), are
not necessary for a typical ectodermal folding. On the other hand, the ectodermal
cells of separated parts are contracted 1.5 to
2 times in relation to analogous cells of
non-dissected zones; that shortening can be
due to tonofibrillar contraction only. The
majority of contracted cells become triangular, their bases forming the convex
surfaces of the folds (Fig. 2A,B). The
lateral sides of the triangular cells are
closely fitted to one another, which results
in the formation of the characteristic "cell
fans" near the cut surfaces of the separated
122
L. V. BELOUSSOV AND J. G. DORFMAN
parts of the epithelium. This result shows
that the initial tight package of epithelial
cells tends, after dissection, to become as
loose as possible under the given mechani-
FIG. 1. Experiments on D. pumila rudiments illustrated in frontal sections. A, Normal growing tip
with symmetrically bent LR's. B,C, Vertical growth
of LR's after removal of CR. D, Inclination of CR.
towards the removed right LR. E, "Vtrticali/ation"
of left LR and normalization of cell orientation in
the left wall of CR after the insertion of celloidin
membrane (cm.) . F, The beginning of cell normalization (n) in right wall of CR after dissection
of the right LR (indicated by arrow) . G, Folding
of separated roof ectoderm (s.r.ect.) of CR in 2
lo 4 min after operation, imitating normal morphogenesis. (A-D from Beloussov, 19G5.)
MECHANICS OF HYDROID MORPHOGENESIS
SOmlm
723
their coenosarc is alternately propulsed
(extended) and retracted (for reviews and
references, see Wyttenbach, 1968, and
Beloussov et al., 1972) .3 By means of time
lapse cinephotomicrography (exposure intervals of 1 to 5 sec), it became possible
to obtain some data which permit elucidation of the mirro-mechanisms which give
shape to the rudiment during growth. It is
convenient to describe first the process of
longitudinal stem growth and follow this
with a description of hydranth morphogenesis, although both will be shown to
be based on what are probably identical
mechanisms.
Longitudinal growth
FIG. 2. Two examples of rapid folding of the roof
ectoderm of a D. pumila CR: after its separation
from the entoderm (A) and, in addition, from
the basal parts of the ectodermal cells themselves
(B) . S.ect. = separated part of ectoderm (note a
considerable contraction of its cells when compared
with a non-separated area) ; ent = entoderm;
b.p.ect. = basal parts of ectodermal cells, containing myofibrils.
cal limitations. Thus, the intact cells must
be mechanically pressed together in the
normal situation.2
TIME LAPSE STUDIES OF INTERMITTENT
GROWTH AND MORPHOGENESIS IN
HYDROID POLYPS
It is at present well known that growth
and morphogenesis in hydroids are of an
intermittent (pulsatory) character; that is,
2 Entodermal cells in similar experiments also
contract, leading to the rolling of a separated fragment; however, this process takes 15 to 30 min
instead of 2 to 3 min as in ectoderm.
Our main attention was focused on the
behavior of the ectodermal cells. Let the
end of a retraction phase be the initial
time point of our description. At this moment, the ectodermal cells are oriented
obliquely, their external ends pointing
upwards (Figs. 3A, 4A). The most pronounced sign of the immediately following
propulsion phase is the upwards shift of
the large area of basal membrane. In growing stems of O. loveni the shifting spreads
far proximally, whereas in hydranths it is
limited at the proximal end of the rudiment by the developing diaphragm. In
D. pumila CR's, the proximal border of
the shifting area coincides approximately
with the level of the LR's.
During the first part of the propulsion
phase (about one-third of its total duration in Obelia stems, or roughly 1 min),
the basal membrane and the whole entodermal column along with the attached
internal ends of the ectodermal cells shift
upwards (distally) as a single solid body;
the rudiment's tip shifts upwards at the
same rate. The external ends of the ectoderm cells remain at the same time fixed
to the perisarc. This naturally leads to a
3
The first author who descrbied growth and
shaping pulsations in marine Hydrozoa was, apparently, Russian zoologist K. Saint-Hilaire (1930) .
724
L. V. BZLOUSSOV AND J. G. DORFMAN
A
B
FIG. 3. A scheme of ectodermal cell shifts and
reorientations during growth pulsation in an
O. loveni stem. A-D, Successive phases of growth
cycle, ht-perisarc; pi = plasmalemma. The arrows
indicate directions of shifts subsequent to the phase
shown. Stippled contours indicate the localization
of supporting structures at the phase shown. E, A
scheme of cell shifts during the giowth cycle.
1-3 = successive positions of a cell; u.b.m. = upwards shift of basal membrane; d.b.m. = downwards shift of basal membrane; u.pl. = upwards
shift of plasmalemma.
more-or-less complete "normalization" of
the ectodermal cell orientation with respect
to the basal membrane (Figs. SB, 4B).
During the last two-thirds of the propulsion phase (about 2 min for Obelia), the
rigid character of the upwards shift is
disturbed. The more proximal regions slow
down their motion earlier than the distal
ones, giving the impression that a "stopping-wave" spreads in a proximo-distal
direction. At this time a transverse broadening of the Obelia stem is taking place at
some distance below its tip. In D. pumila,
each upward shift of basal membrane and
entodermal column starts from the most
proximal level and gradually spreads
distally.
After a pause (approximately 1 min in
Obelia), a downwaid shift of the basal
membrane begins, accompanied by a shift
of the attached internal ends of the ectodermal cells. This shift begins in both
species from the proximal regions (Fig.
3B) and spreads distally (upward) (Fig.
3C) with the rate around 30 microns per
minute in Obelia and 50 microns per minute in Dynamena. The total duration of
the retraction phase in both species is
around 3 min. The tip of the rudiment at
this time also moves downwards. At the
end of the retraction phase in a majority
of pulsations (but not in all) a prominent
process of rapid (taking no more than
0.5 min) upward shifting of the external
ends of the ectodermal cells takes place
(Fig. 3C). Then the next propulsion phase
begins. The whole scheme of cell shifting
and reorientation during the growth cycle
is presented in Figure 3£. The behavior
of the entodermal cells is generally similar to and approximately synchronous
with that of the ectodermal cells.
Changes of cell orientation and cell
length are particularly visible in histological sections (Figs. 5, 6, 7). In both species
the angle of cell orientation with respect
to the basal membrane changes from 30 or
40° (retraction phase, Figs. 5/4, 6A, 1A)
to 90° (propulsion phase, Figs. 5B,C, 6B,
IB), whereas the length of the ectodermal
cells decreases at the same time by 1.5 to
2 times. This demonstrates that not only
normalization of cell orientation, but also
considerable cell contraction, is taking
place during the propulsion phase. Correspondingly, cell relaxation takes place
during the retraction phase. Another noteworthy process, easily reconstructed his-
MECHANICS OF HYDROID MORPHOGENESIS
725
tologically, is the "repacking" of ecto-
dermal cells during their normalization.
FIG. 4. Frames of different phases of growth and
shaping pulsations in an O. loveni stem (AJi) and
a D. pumila CR, frontal view (CyD). A,C, Retraction. B,D, Propulsion phase. In A and B, cell
orientation in the left lateral wall is indicated.
Note a marked distolateral protuberance in D
(dl.p.) as contrasted to the smoothness of CR
contours in C. Time duration between A and B is
200 sec; between C and D, 270 sec.
726
L. V. BELOUSSOV AND J. G.
FIG. 5. Histological pictures of different phases of
growth pulsations in 0. loveni rudiments. A-D,
Successive phases of growth pulsations in a stem
(compare with Fig. 3A-C). The arrows indicate
the directions of successive shifts (in C and D the
DORFMAN
upward shift of the external ends of ectodermal
cells is taking place). E, Rudiment of hydranth
during contraction of cells of its distal half (in
the proximal parts a downwards shift begins).
MECHANICS OF HYDROID MORPHOGENESIS
oq
FIG. 6. Frontal section pictures of successive phases
of growth pulsations in a D. pumila CR. A, Retraction (cell relaxation). B,C, Propulsion phase,
lateralward shifts at the distolateral angles and
downward shifts in the proximal regions. D, The
beginning of the next retraction phase. The arrows
indicate directions of successive shifts,
728
L. V. BELOUSSOV AND J. G. DORFMAN
Rudiment shaping
Time-lapse observations of developing
hydranth rudiments give the impression of
a great number of seemingly independent
motions of different parts, among which
one of the most visible is the periodical
contraction-extension of the proximal zone
of coenosarc (Hale, 1960; Beloussov et al.,
1972). However, only the processes taking
P
SOM/M
part in molding the distal-most, still soft,
perisarc (which, upon hardening determines the specific shape of "formed" rudiments) are of real morphogenetic significance. Movements of the proximal
coenosarc zone do not belong to them. On
the contrary, the most important "molding" movements are the successive outward
pushes of the disto-lateral coenosarc regions (Fig. 4C,D; see Fig. 5 in Beloussov
et al., 1972). Each of these pushes lasts
around 1 min, is of 5 microns (Dynamcna)
or 1 to 2 microns (Obelia) in amplitude,
and regularly takes place during each
FIG. 7. Details of histological structure of D. growth cycle immediately after the cells
pumila CR at the opposite phases of growth pul- of a given level become orientated norsations. Afi, Similar areas of the lateral ectodermal
wall of CR during retraction and propulsion phases mally to the surface. (In D. pumila the
respectively (compare with Fig. §AJi) . C,D, Disto- interval between passage of the "starting
Jateral angles during retraction and propulsion
wave" through a given level and the out(outward "push") respectively (compare with Fig. ward push lasts approximately 1 min.)
4CJO) . Note cell contraction in B and D and ex- According to histological data, at the motension in A and C. pi = plasmalemma; b.m. =
basal membrane. The disto-proximal direction is ment of the outward push, ectodermal cells
of the disto-lateral protuberances contract
indicated (DP) .
and become triangular (a behavior mimicking the previously mentioned results of the
That is, by comparing Figure 7A with IB, dissection experiments), and the density
one can see that in order to obtain the of their arrangement decreases (Figs. 6C,
transformation of A to B, the cells have ID). During the retraction phase, they
to slide upon one another, thus trans- elongate and their density returns to the
forming a "multirowed" (pseudo-strati- initial level (Figs. 6D, 7C).
fied) epithelium to a "unirowed" (columnar) one. A similar rearrangement of
contracting ectodermal rudiment tip cells Counterphase character of groiuth
leads to the expansion of the entire roof pulsations in adjacent walls of
of the rudiment, which is evidently geo- neighboring central and lateral
metrically inevitable and is especially well rudiments in D. pumila
pronounced in Obelia (Fig. 5, compare
A, C, and E). In the entoderm also, the
In 38 out of 50 successive pulsations
process of cell normalization-denormaliza- traced in as yet undiverged CR and LR's
tion is well expressed but that of cell of D. pumila, an upward shift of the basal
contraction and sliding-repacking is less membrane in the CR wall clearly coinpronounced.
cided with a downward shift of the basal
MECHANICS OF HVDROID MORPHOGENESIS
membrane in the adjacent LR wall, and
vice versa. The whole process resembles
the back and forth pulling of a rope thrown
over a crossbeam. Indeed, due to the continuity of the basal membrane between the
two rudiments, an upward shift in one
clearly prevents or diminishes the amplitude of the shift in the same direction in
the other. Such a characteristic of the
process points up the possibility of some
sort of feedback relationship between the
amplitude of the preceding pulsation and
the time of the beginning of the next one.
On the other hand, it must be stressed that
due to "counterphase activity," a more
oblique cell orientation is established in
each rudiment than in the absence of such
interactions. It should be recalled that,
after removal of a rudiment or breaking
of the structural contacts between two
rudiments, the orientation of cell axes in
the remaining rudiment becomes more perpendicular to the rudiment's surface in just
a few minutes after the operation. The
consequences of this situation will be
analyzed below.
MECHANISMS INVOLVED IN THE GROWTH
PROCESS
Active forces
Cell contraction-extension during propulsion-retraction phases as well as simultaneous cell reorientation (normalizationdenormalization) may be interpreted as
the natural results of tonofibrillar contractions of tightly packed cells. To imitate the
729
situation in the lateral wall of a growing
rudiment, take a group of such cells initially orientated obliquely (parallelogramshaped) as in Figure 8. According to histological data, cell volumes do not change
considerably during their contractionextension. It is easy to see that the only
way to decrease their lengths (i.e., to contract to some extent) without altering their
volumes at the same time and without increasing their diameters (which is prevented by the pressure of symmetrically
situated neighboring cells) is to transform
their shape toward a rectangular one. Indeed (see Fig. 8), OL < OP (contraction),
while SRN0L = SMNOp (where S equals volume) and RL = MP (constancy of diameter) . One can see that the transformation
of cell shape from parallelogram-like to
rectangular corresponds to the tangential
shift of one surface with respect to another
(Fig. 8, arrow from P to L). Therefore,
all observed cell shifts closely connected
with growth processes can be interpreted
as being due to the action of tonofibrillar
mechanisms. On the other hand, a detailed
analysis demonstrates that no kind of myofibrillar contractions (either transverse or
longitudinal) can lead to similar results.
Passive and supporting structures
In order to lead to progressive stem
growth, the contracted-normalized cells
must be integrated into a single mechanical system by means of some supporting
and binding structures, some of which possess elastic properties. First of all, for the
basal membrane and stem tip to shift upwards without shifting the plasmalemma
downwards at the same time, the ectodermal column must have a support on its
periphery somewhere below the tip. Obviously, a supporting role is played here
M
Kp
„ L
by perisarc (Fig. ?>A,B, dotted area). This
FIG. 8. A theoretical scheme of normalization of
initially parallelogram-shaped cells in a lateral wall assumption does not require any specific
of a growing rudiment. Solid lines—initial cell mechanisms of cell-perisarc or plasmapositions; dotted lines—their positions after con- perisarc connection, since the very increase
traction (the latter is indicated by three pairs of
in diameter of the coenosarc during cell
arrows inside each cell) . Arrow P —> L indicates contraction (Fig. 9A,A,) promotes close
the direction of a shift of the lower surface of the
contacts and, thus, a considerable tangenlayer as a result of cell contraction.
730
L. V. BELOUSSOV AND J. G. DORFMAN
MECHANISMS INVOLVED IN MORPHOGENESIS
tial "friction" between both structures. At
the end of the propulsion (roof extension)
A simple regularity can be easily formuphase the plasmalemma of the tip region lated as a result of the film analysis: The
is stretched, and thus accumulates certain more a given area is evaginated, the greater
elastic energy. The conditions for the re- is the amplitude of its outward pushes,
lease of the energy seem to appear later, deforming the perisarc and, in turn, leadnamely at the retraction phase. At that ing to the progressive sharpening of the
time, due to cell relaxation (and thus to surface features of the rudiment. The fola decreasing of coenosarc diameter), the lowing set of simple mechanical examples
plasmalemma detaches from the perisarc; illustrates the situation.
the only point where it remains closely
Let us consider apical areas of different
connected is at the stem tip (Fig. ?>C,D,
shapes, all of them enveloped by plastic
dotted area). Under such conditions
perisarc and elastic plasmalemma and
the elastic contraction of the previously
composed of a layer of normally orientated,
stretched plasmalemma pulls and shifts the
tightly packed cells, periodically contractectodermal cells upwards at their external
ing along their axes. During contraction,
ends.
they obviously push one another in lateral
Therefore, we assume that besides the directions, and thus the total surface area
active force of cell contraction, a passive of the layer tends to increase. The geoforce of elastic plasmalemma contraction metrical result of their contraction will
plays a necessary role in progressive growth. depend largely upon the initial shape of
It is important that the anchoring points the rudiment being considered:
be shifted during each growth pulsation:
1) If the initial transverse section of an
During the propulsion phase the support- apical area is circular (Fig. 9A), an outing role is played by subapical perisarc, ward pressure, caused by simultaneously
whereas during the retraction phase it is contracting cells and applied to the periplayed by the apical area (which is pos- sarc, can lead to a stretching outward of
sible due to that area's crush-resistant arch the plastic perisarc and to expansion of
form).
the rudiment without altering its circular
V\C 9. A scheme of geometrical transformations of
rudiments with different initial shapes. Crosssections are presented. A,B,C, Initial rudiments.
Arrows indicate the results of their transformations
(A, and A, for A; Ji, for B; B for C) . b,, bt, A
scheme of forces applied to a cell in convex and
concave regions of the B rudiment respectively.
731
MECHANICS OF HYDROID MORPHOGENESIS
shape1 (Fig- 9A,) • One can see, however,
that if the layer's thickness is sufficiently
small, the circularly symmetrical shape will
be mechanically unstable; that is, a small
(accidental) local deformation leads to
progressive ruffling of the layer (Fig. 9A2).
The ruffled shape thus produced is mechanically much more stable. The number
and exact shape of the resulting symmetrically arranged folds are determined by
mechanical parameters of the layer.
2) If a given rudiment initially possessing several concave areas at relaxation
(Fig. 9B) is considered at the moment of
cell contraction, any cell situated in a concave area will be subjected to lateral pressure forces applied to it from neighboring
cells, forces that will be directed away from
the perisarc (Fig. 9b2). Similar forces
applied to a convex area will be directed
towards the perisarc (Fig. 9b,). These
forces will thus further sharpen the initial
surface relief of the rudiment5 (Fig. 9B,).
3) Taking a rudiment of intermediate
shape, that is, one possessing areas of both
low and more sharp positive curvature
(Fig. 9C), during the contraction phase
a tendency toward extension of the surface
layer can either stretch the perisarc, producing a general expansion of the whole
rudiment without altering its shape, or
lead to inward folding (and thus divergence from the perisarc) of the less convex
areas, producing a situation similar to that
shown in Figure 9B. It can be easily demonstrated that, using the given geometrical
assumptions, the first situation is impossible because of mechanical instability,
since at any intermediate point a small
accidental deformation will switch the
process over to the second situation. Therefore, as in the previous example, the rudiment's contour will become more pro-
4
A very similar scheme, applied however only to
the reversibly contracting (detached from perisarc)
subapical region of stolon and hydranth, was proposed by Hale (1960; see his Fig. 5).
5
A progressive growth and stability of depressions is provided by a constant addition of new
layers of perisarc by an inwardly folding cell layer.
nounced while the order of its symmetry
remains the same.
A great number of morphogenetic processes in which the resulting shape of the
perisarc is directly determined by momentary changes of shape of the tip region at
successive propulsion phases may be interpreted by similar considerations. Examples
are: the formation of an Obelia daughter
stem at the convex side of the maternal
one (Fig. \QA) ; the main features of morphological differentiation of an Obelia
hydranth as it changes from a shape with
smooth contours (Fig. 10B); and the set
of transformations characteristic of Dynamena morphogenesis (Fig. 11; see Beloussov and Dorfman, 1972, for details). In all
these cases, the morphogenesis is characterized by progressive inward folding of concave or, at least, less convex areas, and
further evagination of sharply convex areas.
The situation shown in Figure 9A2 seems
also to occur in the course of Obelia hydranth development. A young hydranth
A
C
D
FIG. 10. Geometrical transformations in Obelia. A,
Origin of daughter stem. B, Differentiation of
hydranth. CJ), Schematical drawings of two successive stages of hydranth ruffling leading to tentacle formation (transverse sections). Cell nuclei
are represented, b.m. = basal membrane.
732
L. V. BELOUSSOV AND J. G. DORFMAN
FIG. 11. Schematical drawings of a scries of transverse sections of a normal D. pumila colony, arranged in proximo-distal direction (A-F) , aberrant
variants in cross-sections {G-H) , and lateral view
of a colony indicating the levels corresponding to
drawings A-F. Positions of sagittal and frontal
planes are also indicated. A-F present at the same
time the successive stages of development of an
outgrowth. The forms B,DJ?,H may be directly
derived from the forms A,C,E,G respectively,
analogous to Fig. 9A,B. (Modified from Beloussov
and Dorfman, 1972.)
with relatively small diameter and thick
walls expands uniformly, whereas later on,
after considerable expansion and thinning
of the wall, ruffling of the layer takes
place, resulting in tentacle formation (Fig.
10 C,D).
oblique cell orientation over that on the
side with the more normal one geometrically inevitably leads to corresponding differences in the elongation rates of the two
walls and to bending of the rudiment. One
can see now that the examples of regular
correlations between cell orientation in a
rudiment and the direction of its subsequent bending ("prognostical" cell orientation mentioned above) are in full agreement with this mechanical interpretation.
A number of normal and experimentally
modified processes of D. piunila morphogenesis can be interpreted in an analogous
manner. A common starting point here is
the phenomenon of counterphase activity
of adjacent LR and CR walls, promoting
the obliqueness of cell orientation in both
rudiments at the relaxation phase. The
cells of all other walls of the rudiments
obviously have a more normal orientation
at the same phase. Finally, it is evident
(and experimentally verified) that after
separation of CR and LR's, cell orientation
MECHANISMS INVOLVED IN BENDING
As one can see from the above discussion, cell normalization during the propulsion phase leads to an upward shift of a
certain amount of cell material. Obviously,
the more oblique the initial cell orientation, the greater this shift will be. At the
same time, the greater the amount of cell
material transported to the apical region
per propulsion phase, the greater will be
the stretching of the tip perisarc. Similar
considerations may be used for analysis of
the growth direction of a rudiment with
asymmetrical cell orientation in its lateral
walls. The predominance of stretching of
tip perisarc on the side with the more
MECHANICS OF HYDROID MORPHOGENESIS
in their adjacent walls becomes more normal. From these facts, the following can
be clearly derived:
1) Lateral bending of the LR's is a
direct consequence of an asymmetry of cell
orientation in the LR walls caused, in turn,
by the "counterphase interactions" with
the adjacent CR.
2) Expansion of the CR in the frontal
plane (i.e., laterally) but not in the sagittal plane (Beloussov et al., 1972) is due
to the above-mentioned differences in cell
orientation in the respective walls at the
relaxation phase. The upward transport of
cell material along frontal (lateral) walls
and therefore the amplitude of outward
pushes along these walls exceed the cell
transport and amplitude of the pushes
along the sagittal walls. This naturally
leads to predominant CR extension in the
frontal plane.
3) Vertically orientated growth of the
LR's after removal or separation of the
CR is apparently clue to cessation of the
"counterphase interactions." This leads to
cell normalization in the median LR walls,
thus producing a symmetrical cell orientation in these rudiments.
4) Unilateral removal of the LR leads
to cell normalization in the CR wall adjacent to the removed LR. Thus, an asymmetrical cell orientation is established in
the CR, which leads to its bending according to the above considerations.
CONCLUDING REMARKS
Any mechanical process which takes place
in a system with variable mechanical
parameters is completely determined by:
(i) the initial geometrical configuration
of the system and the initial pattern of
mechanical stresses, (ii) the external mechanical influences and restrictions during
the process, and (iii) the spatio-temporal
distribution of mechanical parameters in
the system. As it pertains to asexual generation of hydroids, the spatial distribution
of external mechanical influences as well
as of mechanical parameters of the system
itself may be regarded as homogeneous.
733
As to the temporal pattern of the mechanical properties of coenosarc, its periodicity
is quite obvious and seems to be the necessary condition for a constant progressive
growth. Morphogenesis of such a system
will be determined mainly by the initial
geometry of a rudiment. It is worth mentioning that, at certain stages of development, the geometrical configuration of a
rudiment is mechanically unstable, making
possible, particularly, a decrease in its
symmetry as well as the subdivision of a
structurally and geometrically homogeneous rudiment into sharply separated
regions (transformation of the circular
symmetry of an as yet non-differentiated hydranth into the radial symmetry of a
tentacle whorl, differentiation of a Dynamena CR into three parts, etc.).
The proposed point of view may be considered as a particular case of "positional
information" concepts (Wolpert, 1969),
since in analyzed systems such "positional"
parameters as curvature of cell layers, cell
orientation, the relation between the diameter of a rudiment and the thickness of its
walls, etc., are morphogenetically decisive.
In our examples, a cell "feels" displacements and deformations produced by other
cells in the rudiment in so far as it is
embedded in the stress and strain field
caused by the activities of these cells. Unlike other, similar concepts, the dependence of cell "behavior" on the "positional
information" available is assumed by us to
be determined by mechanical laws.
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