Coordination in Sponges.
The Foundations of Integration.
MAX PA VANS DE CECCATTY
Laboratory of Histology, University Claude Bernard, 43 Bd. du 11 Novembre,
69621 Villeurbanne, France
SYNOPSIS. Coordination mechanisms in sponges involve not only epithelia but also the
meser.chynie, which is the basic internal milieu for aii primitive Metazoa.
There are three main types of coordination pathways: (i) Fluid extracellular coordination pathways are used for the spreading of materials through the mesenchymal connective matrix. Examples are provided by the processes of wound healing, regeneration,
gametogenesis, and gemmulation. (ii) Mobile cellular coordination pathways follow the
transitory contacts and consecutive exchanges performed by amoeboid cells which wander
in the mesenchymal matrix. Examples are provided by the processes of cell reaggregation and morphogenesis, (iii) Fixed tissue coordination pathways are achieved by permanent connections between cells belonging to the same unit structure, which can be an
epithelium or which can be composed of mesenchymal cell networks and bundles. Examples are provided by contractile activities of oscular membranes, internal canals, or
of the whole sponge. The first and the second pathways do not undergo significant modifications in the various species of sponges. The third pathway, and especially the mesenchymal contractile tissue, appears to be significantly well developed only in thick-walled
sponges.
The discussion compares the three coordination systems of sponges with integrative
systems in higher Metazoa. The conclusion is that if the coordination mechanisms in
Porifera do not quite resemble those found in higher animals, nevertheless they would
have been suitable for a further advent of true hormonal, immune, muscle, and nervous
systems such as we know in other Metazoa.
A sponge is a filtering sac whose life mode
seems to be reduced to a simple operation:
circulation of the surrounding water
throughout the body so as to obtain what is
necessary for growth and reproduction.
This "behavior" is of such a simple pattern that it obscures the complexity of the
processes which support it. Hence, the
sponge is considered as a pump constructed
in such a way that the mechanical beating
of the flagella lining its cavities is sufficient
to introduce water via small incurrent openings, the pores, and then to expell the same
water by a larger excurrent opening, the
osculum. In this mechanical system the
flagellated cell, the choanocyte, is essential,
all the more so as it retains the potential
These studies are supported by the Centre National de la Recherche Scientifique (ERA 183),
Paris. All the members sharing in the work of the
Recherche Cooperative sur Programme n° 248 are
gratefully acknowledged, particularly J. Pottu, R.
Rasmont, and J. Sube with regard to certain sequences of the film displaying the main data presented in this paper which is dedicated to Professor
Odette Tuzet.
of sexual reproduction for the whole organism, for it is the choanocytes which give
rise to spermatozoa and ova (Tuzet et al.,
1970; Diaz et al., 1973). Such a system makes
it easy to understand why the Porifera are
considered poor relatives of the other
Metazoa. They have made no apparent
major advance. The choanocyte is a cell
type well known in the Protozoa; to have
aligned these cells side by side to form
flagellated surfaces is not even original
when we consider the colonial Protista.
However, for zoologists this apparent simplicity is a trap.
In fact, a sponge is a sac consisting of two
epithelial layers. The outside layer has its
own cells, the exopinacocytes, in the same
way as the inside layer has its own endopinacocytes and choanocytes. All these cells
are in direct contact with water. However,
between these two walls there is an enclosed
space which is not in direct contact with
water and which forms a true internal
milieu, the mesenchyme. Certain properties of this mesenchyme (in particular the
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MAX PA VANS DE CECCATTY
ionic extracellular concentrations) are not (Pavans de Ceccatty and Tuzet, 1958;
very different from those of the external Pavans de Ceccatty, 1962). Moreover, exenvironment. In other respects, this milieu periments have shown that when a freshis quite different from the external environ- water sponge of the genus Ephydatia forms
ment and has some obvious features. Here in its mesenchyme a small gemmule which
are found the intercellular macromolecules will function in asexual reproduction, there
which are characteristic of the connective is a sort of emitted signal which orientates,
matrix of all Metazoa, such as collagen and towards the same point of the mesenchyme,
mucopolysaccharides (Gross et al., 1956; the displacement and gathering of amoeGross and Piez, 1960; Garrone, 1969, 1971; boid cells which give rise to the gemmule;
Thiney and Garrone, 1970; MacLennan, this process can be experimentally triggered
1970) as well as cells independent of the by theophylline (Rasmont, 1973).
two neighboring epithelia.
Thus, it appears that certain materials
Porifera are composed of epithelia and given off by cells can spread throughout the
mesenchyme (Hyman, 1940). If it were connective matrix and act upon other cells
necessary to designate the point of struc- which they reach. Transmission radiates
tural departure from the Protozoa to the outwards from the source and is susceptible
Metazoa, it is not in the arrangement of the to the usual diffusion factors: distance,
multicellular epithelial layers where it must fluidity, and physical hindrance of the
be sought, but in the organization of the matrix. These factors result often in a
enclosed internal milieu in the form of gradient which is capable of orientating
connective mesenchyme which has been cellular responses. This coordinating system
judiciously designated elsewhere as the is based on the endocrine capacities of cer"archihiston" (Steinbock, 1963).
tain cells, on their ability to react to certain
Hence, in spite of the simplicity of the products, and on the efficiency of diffusion
life mode of a sponge, the coordination operating under the control of the macrosystems necessary to this organism will de- molecules of the connective matrix. Indeed,
pend on the mesenchyme as well as the the secretory activities of mesenchymal cells
epithelia (Pavans de Ceccatty, 1974). Ac- have been shown by means of electron micording to the pathways they use, these croscopy (Pavans de Ceccatty et al., 1970;
coordination systems can be grouped into Pavans de Ceccatty, 1971, 1973). In addithree types which are: (i) the fluid extra- tion, pharmacological experiments revealed
cellular system, (ii) the mobile cellular sys- specific cell reactivities to certain substances
tem, and (iii) the fixed tissue system.
such as theophylline (Rasmont, 1973),
acetylcholine, and epinephrine (Pavans de
FLUID EXTRACELLULAR COORDINATION
Ceccatty, 1971). Some of these substances
PATHWAYS
occur naturally in the tissues of sponges,
for example, catecholamines and serotonin
When after lesion, in Hippospongia or (Lentz, 1966; Bergquist, personal communiother sponges, there is wound healing of a cation) or the "gemmulostasine" which insurface area followed by regeneration, the hibits the hatching of gemmules (Rozenfeld,
cellular dedifferentiation and reorganiza- 1970).
tion processes extend in depth along a
Hence, there exists in sponges fluid extragradient from the surface to the interior of cellular coordination pathways used for the
the mesenchyme (Korotkova, 1970; Thiney, radial spreading of messenger materials.
1972). In the same way, when flagellated
chambers are transformed into male or fe- MOBILE CELLULAR COORDINATION PATHWAYS
male gametocysts in Hippospongia (Fig.
I A), the general structure of tissues and the
Time-lapse cinematographic recordings
equilibrium between different cell types are (for example, at speeds of 1 frame/sec) have
modified following a gradient around each shown a multiplicity of apparently disorgametocyste through the mesenchyme ganized cellular displacements which take
COORDINATION IN SPONGES
place continuously in the mesenchyme of
some sponges suitable to in vivo observation
(Ephydatia: Pottu, 1973; or Halicondria:
Sube, 1973). When Ephydatia's gemmules
hatch, morphogenesis begins by the differentiation of two pinacocytes sheets, and it
continues between these sheets within the
mesenchyme in which numerous multipoleiu amoeboid ceils, the archeocytes, wander. New cellular differentiations take shape
gradually during these amoeboid displacements which cause transitory intercellular
contacts (Fig. IB). Of those cells involved,
we can distinguish two categories: firstly,
those that remain mobile, such as all types
of amoebocytes and the lophocytes which
produce bundles of collagen fibers, and
secondly, those cells which associate and
become attached to form internal canals
and flagellated chambers. The number and
categories of wandering cells decrease in the
adult sponge, that is, during its "morphostasis" which could be defined as the dynamical stability of structures, the cells of
which are always able to move. Indeed, in
the adult sponge there is a persistence of
the wandering process which regulates the
continually renewed dynamic equilibrium
between the cellular categories (Levi, 1970;
Borojevic, 1970, 1971; Rozenfeld and Rasmont, 1973).
So it can be seen that the connective
mesenchyme is not only responsible for the
spreading of messenger materials, but also
provides the substratum of a closed space
limiting the field of migration for mobile
cell displacements. In this closed connective
space, the cellular behavior falls into clearcut categories and leads to distinct anatomical structures. The migrating capacities of
cells inside the mesenchyme have been
shown by microcinematography as discussed
previously. Further evidence has been provided by isotopic labelling in Ephydatia
(Rozenfeld and Rasmont, 1973) as well as in
Chondrosia, in which epithelial cells can
leave their tissue and penetrate the connective matrix, where they are transformed
into lophocytes producing collagen (Pavans
de Ceccatty and Garrone, 1971). During
these cell displacements numerous transitory contacts between different cells are
897
observed. Electron microscopic studies indicated possible cell-to-cell transfer of material in Ephydatia (Pottu, 1973) and in
Haliclona (Pavans de Ceccatty et al., 1970).
Moreover, information exchange at the moment of cell contacts has been reported in
studies on cellular aggregation, which involves cooperating cells exhibiting a definite
mechanism of interaction of their surfaces
(Moorkerjee and Ganguly, 1964). The information is related to certain molecules,
certain "factors" of cell surfaces, such as
factors supporting specific cell aggregation,
selective adhesion, or reciprocal inhibition
between cells of different species (MacLennan, 1969, 1970; Humphreys, 1970;
Curtis and Van de Vyver, 1971; Van de
Vyver, 1971, 1973). Finally, during morphogenesis, cell surface movements are responsible for extending affinities revealed by
contacts between cells which differentiate
to form sponge architecture (Moorkerjee
and Ganguly, 1964).
Sponges are therefore seen to have mobile
cellular coordination pathways which follow the random contacts between amoeboid
cells.
FIXED TISSUE COORDINATION PATHWAYS
In vitro studies have shown that electrotonic coupling exists in Microciona cell
populations (Lowenstein, 1967). Hence, direct transfer of ions and small metabolites
is possible between sponge cells. On the
other hand, optical microscope studies using
silver impregnations of Tethya, Hippospongia, and Euspongia (Fig. ICJ2) have
revealed the existence of deep lying mesenchymal bundles and networks in which
the cells are connected together and to
adjacent epithelia by means of fine cellular
processes and terminal junctions (Pavans de
Ceccatty, 1959). In the same species, pictures
obtained by electron microscopy have also
shown close membrane appositions between
neighboring cells (Fig. IE) and transfer of
vesicles or materials from one cell to another (Pavans de Ceccatty, 1966a,b; Pavans
de Ceccatty et al., 1970).
In species with highly developed mesenchyme, such as Tethya, Hippospongia,
898
MAX PAVANS DE CECCATTY
COORDINATION IN SPONGES
899
Euspongia, or Verongia (Vacelet, 1966),
Tedania, Microciona (Bagby, 1966), and
Hamigera (Boury-Esnault, 1972), the cells
of deep mesenchymal networks show
muscle-like differentiation, in accord with
the high level of contractile activities in
these sponges. No electrical phenomena related to these activities has been experimentally displayed up io now (Prosser et al.,
1962; Prosser, 1967). However, kymographic, photographic, and cinematographic recordings allowed spontaneous or
provoked activities to be analyzed (Emson,
1966; Prosser, 1967; Pavans de Ceccatty,
1969; Reiswig, 1971). These contractions
are sometimes rhythmic, always slow (the
fastest last for 30 sec) and are either limited
to restricted groups of a few cells or propagated by waves over large zones. Hence, we
can observe coordination of some areas
which, by their phasic or maintained contractions, act directly on the water circulation in the canals and on the displacements
of materials and cells in the mesenchyme
within the field of contraction (Pavans de
Ceccatty et al., 1960; Pavans de Ceccatty,
1969). Physiological studies of the pumping
activities of the sponges Verongia and
Tethya have shown that the variations of
the contraction states of the osculum and
canals are coordinated with the activities of
the flagellated chambers in such a manner
as to maintain a constant velocity of removal of exhalant water in relation to the
beating frequencies of flagellated choanocytes (Reiswig, 1971). This proves that there
is a propagation and an extension of information throughout the whole sponge
(over a distance of several centimeters covered in 4 to 6 min). Propagation is carried
out from cell to cell by means of connections which are no longer transitory contacts as they were for the mobile cells. These
connections are specific junctions of fixed
cells belonging to the same unit structure,
which can be epithelial, constituted of
pinacocytes, or which can be reticulated as
in the mesenchymal contractile tissue in the
form of loose lattices or of bundles. The
cells of mesenchymal contractile tissue correspond to the same cell line as that of the
epithelial pinacocytes, which are themselves
often contractile.
Sponges are thus seen to possess fixed coordinating systems which use permanent
connections between cells of the same tissue.
This system is based on the capacity of cells
to build a relatively stable structure and to
carry out direct exchanges from cell to cell
according to structurally defined pathways.
So, a group of cells may control its own
activities and also coordinate the activities
of other cell groups which are found at its
input and output, such as choanocyte chambers on one side and osculum on the other
(Fig. 2). In Porifera, experiments and observations have shown that these coordinating pathways involve epithelia and also
intramesenchymal populations of contractile cells. In these fixed coordination systems
there is always the participation of the internal connective matrix, either providing a
metabolic environment (at least partially
for the epithelial cells of which one pole is
in contact with water), or providing an
anatomic and physiologic arrangement
which may allow reticular formations of
contractile cells to develop in depth.
This anatomical role of the mesenchyme
in sponges is of major importance (Brien,
1943). In fact, if all sponges possess epithelia
able to support fixed tissue coordination
pathways, only certain sponges with thick
mesenchymal walls would seem to have contractile internal networks or bundles, which
are pathways additional to those of epi-
FIG. 1. A, A gametocyst containing an egg (E),
surrounded by different cell types modified along a
gradient through the mesenchyrae in Hippospongia
communis. Flagellated chambers have disappeared
and many dedifferentiated and pigmented cells
are gathered near the gametocyst. Hematoxylin.
X 700. B, Transitory contacts (arrows), by means
of large appositions or fine processes between wandering cells in the mesenchyme of living Ephydatia
mulleri. Phase contrast, x 1450. C, Myocyte-like
cell bundles (B), in contractile area of the
mesenchyme (M) near flagellated chambers (FC),
in Hippospongia communis. Trypan blue. X 600.
D, Network of rayocyte-like cells (arrows), in contractile area of the mesenchyme (M), in Tethya
lyncurium. Silver impregnation, x 750. E, Electron
micrograph of several types of junctions and close
contacts (arrows) between a cell body and processes
in a mesenchymal cell bundle surrounded by collagen matrix (M) in Euspongia officinalis. X 12,000.
900
MAX PAVANS DE CECCATTY
Thin
walled
Sponges
FIG. 2. Theoretical diagram of a sponge and its
coordination systems. The organism is in contact
with water (arrows) by its exopinacocytes on the
exterior, its endopinacocytes covering the incurrent
(ic) and excurrent (ec) canals, and finally by the
central choanocytes (ch). Three sectors are represented, from left to right, symmetrically with respect
to a horizontal axis. They are representative of the
increasing volume of the mesenchyme which is: (i)
slightly developed in thin-walled species, (ii) of a
greater extent in other species, (iii) well developed
in thick-walled species. The mesenchyme contains
amoeboid and fixed cells, some of the latter showing
fibril differentiation similar to that found in certain
pinacocytes. Mesenchymal (connective) intercellular
matrix contains mucopolysaccharides and collagen
macromolecules and, according to species, spongin
fibers and spicules (not shown here).
The coordination systems correspond to several
Thick
wa lied
Sponges
transfer pathways. The fluid extracellular pathways
are used for messenger substances spreading in the
mesenchyme, the dimensions and the macromolecular obstructions of which increase in thick-walled
sponges, hence making diffusion slower and more
localized. The mobile cellular pathways follow
transitory contacts of wandering cells, the displacements of which become also slower and more localized in thick-walled sponges. The fixed tissue
pathways are supported by permanent cell junctions. In this fixed system, there is little variation
of epithelial coordination in different species. On
the contrary, mesenchymal tissue coordination by
means of contractile cell bundles and networks
(black), appears to be really differentiated only in
thick-walled species. It is possible, however, to see
these mesenchymal formations outlined in versatile
networks of less developed sponges (sector 2).
COORDINATION IN SPONGES
thelia. Deep reticular formations accompany mesenchymal development. At the
higher level of this development it appears
that the fluid pathway and the mobile
cellular pathway become inefficient to
achieve a certain type of mesenchymal coordination which must occur at a relatively
high speed over a relatively large distance.
Consequently, if the coordination by extracellular fluid and wandering cells do not
seem to be able to undergo significant modifications in the various sponge species, the
third pathway, that is, the stable tissue
system and in particular deep lying contractile structures which achieve a motor
coordination, does on the contrary change
and can develop from one species to another
(Fig. 2). It has been reported that this development depends on the anatomy with
thick walls of certain sponges and on the
ecological conditions in which they live
(Reiswig, 1971).
DISCUSSION. THE FOUNDATIONS OF
INTEGRATION
Coordinating mechanisms in sponges are
the manifestation of an organization level
which includes not only epithelial layers
but also the connective mesenchyme which
forms the fundamental internal milieu for
all Metazoa. Information transfer from cell
to cell may thus follow epithelial pathways
but also the pathways offered by the mesenchyme with its extracellular fluid, mobile
cells, and fixed interconnected cells. However, as could be foreseen (Mackie, 1970)
these information-transfer pathways cannot
be distinguished anatomically from metabolic-transfer pathways. In Porifera, we
cannot characterize elements strictly specialized for signal emission or conduction.
Endocrine secretion is not the prerogative
of a defined category of cells. Amoeboid
movements and transitory contacts can be
displayed by all cells, either permanently
or intermittently. Finally, the epithelia and
the contractile bundles or networks correspond to the organization of tissues which
are as much coordinated for themselves as
they are coordinating for other tissues. Porifera thus have coordination mechanisms
901
and structures which cannot be related in
an exclusive manner to any cell differentiation. The functional cell systems result from
the manner in which cells are organized
amongst themselves at a given moment according to the requirements of development
and homeostasis (Pavans de Ceccatty, 1962).
Because they are ambiguous or versatile,
are these coordination systems in no way
comparable with those of other Metazoa?
Have the more highly evolved animals, beginning with Coelenterates, reinvented
everything on a basis which was, from this
beginning, different and more complex?
Of course, a hormonal system individualized to any extent cannot be attributed
to Porifera. However, the coordination
achieved by radial spreading of messenger
materials controlled by the connective
matrix is the basic modality of such a system, a modality which the sponges in no
way ignore in their gemmulation, gametogenesis, or regeneration.
A cellular immune system cannot be
distinguished in the Porifera as precisely as
that of lymphoblastic transformation or of
tissue specificity can be elsewhere. Nevertheless, coordination achieved by transitory
contacts between mesenchymal wandering
cells and the existence of compatibility or
noncompatibility cellular factors according
to species or strains are the basic modalities
of such a system, modalities which the
sponges in no way ignore for their morphogenesis or for their "morphostasis."
Finally, it is now generally agreed that we
cannot attribute the possession of a true
nervous system to Porifera (Pavans de Ceccatty, 1974). Yet, the coordination carried
out by a reticular tissue which provides
pathways by which the spontaneous or
evoked signals of a definite activity can be
propagated is the basic modality of such a
system, a modality which the sponges in no
way ignore for the regulation of their contractile and pumping activities.
When considering the evolution of integrative systems, and in particular when
considering the origin of the nervous system
(Pantin, 1952, 1956; Passano, 1963; Lentz,
1968; Horridge, 1968; Mackie, 1970; Pavans
de Ceccatty, 1974), the question is to know
902
MAX PA VANS DE CECCATTY
if the search for a stage preliminary to Coelenterates leads eventually to some sort of
reality, or if this search can only be satisfactorily fulfilled by artificial models. Indeed, we find ourselves in the following
situation. Coelenterates possess a true nervous system which is much more complicated than was previously imagined (Ross,
1967). The stage preliminary to Coelenterates can only be conceived under two
aspects: either under the form of unknown
Metazoa, still to be discovered, showing a
simple pre-nervous or neuroid system, still
to be defined; or under the form of already
known Metazoa possessing a coordinating
system, the role and the structure of which
suggest a model which would have been
suitable to the further advent of true muscular and nervous systems such as they exist
in other phyla. The results of studies on
sponges give some support to the second
hypothesis in which the Porifera could be
considered as witnesses of the "pre-history"
of the nervous system. To conclude, if the
coordination in sponges does not quite resemble that found in the Metazoa, it resembles perhaps that of some remote
ancestors of the latter.
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