52
ovary. It is possible, however, that the oocytes of this species
are enlarged mostly through uptake of nutrients from the
coelomic fl uid, as in Membranipora serrilamella (Hageman
1983 ) and Celleporella hyalina (Hughes 1987 ), the oocytes
of which expose part of their microvilli-covered surface to
the coelom remaining embedded in the ovary.
According to the arrangement, structure and size of the
female cells developing in the ovary of brooding cheilostomes, two zones may be delimited: (1) a germinative zone
and (2) a growth-and-ovulation zone. The germinative zone
comprises the basal part of the ovary, i.e. the lower part of the
intraovarian zone limited by the ovary wall of cubic or prismatic cells. It is there that oogonia and previtellogenic doublets occur, most sperm concentrate (and penetrate into the
ovary) and syngamy takes place. Oocytes also increase in
number and undergo the fi rst growth stages there.
The growth-and-ovulation zone comprises the follicle
enveloping the leading oocyte doublet and the uppermost
part of the intraovarian zone directly adjoining the leading
oocyte. This part is represented by a few basal cells and
intercellular spaces between them. The upper and lateral
areas of the follicle wall are composed of fl at (squamous)
cells, while the basal part consists of oval, cubic or prismatic
cells. The main functions of the growth-and-ovulation zone
are the transport of nutrients to the vitellogenic oocyte(s), its
growth accompanied by accumulation of resources, and its
ovulation after maturation.
As the ovary develops and functions, its structure changes
accordingly (see also Dyrynda and King 1983 ). In early ovaries all cells are more or less the same, with differentiation
into wall and basal cells apparently occurring during the
early developmental stages of the fi rst vitellogenic oocyte
and its follicle. The growth of the oocyte is presumably
accompanied by multiplication of ovary cells and changes in
their size and shape; some of the basal and follicle cells
fl atten, whereas the others enlarge and become prismatic or
cuboidal (compare Figs. 1.5A, C and 1.9A, B ). The intraovarian zone gradually fl attens (see Sect. 1.2.4 ).
During and after ovulation, some of the squamous cells of
the follicle apparently degrade. Flat basal cells are no longer
discernible and possibly also degenerate. The follicle walls
“collapse” (see also Vigelius 1882 ) and the intraovarian zone
diminishes considerably. In fact, retention of the ovary during polypide degeneration (sometimes through multiple
recycling) fi ts remarkably well the hypothesis about the
excretory nature of the recycling process (reviewed in
Gordon 1977 ). Contrasting with the adult polypide, which
has no zone of cell proliferation and must degenerate and
regenerate from time to time, oogenetic cycles are accompanied by regular renewal of the cells of the ovary, which may
explain its relative longevity.
There are no essential differences in the structure and function of the ovary in malacostegan and brooding cheilostomes.
In other words, all Cheilostomata have in common a basic
plan of ovarian organization and observed variations
appear to correspond to stages in the evolution of this organ
associated with changes in patterns of oogenesis (see Sect.
3.1.2 ). Any reductions in numbers and size/type of oocytes
would inevitably have resulted in altered gonad structure.
Therefore, one may suggest that differences in ovarian
structure as described above refl ect evolutionary shifts in
oogenesis.
1.3.4 Comparative Analysis of Oogenesis
in Cheilostomata
There are at least three stages in the development of the primary oocyte, from its fi rst appearance to ovulation. A simple
division into previtellogenic and vitellogenic stages (Dyrynda
and King 1983 ) does not quite refl ect the situation. The
descriptive terminology introduced by Chrétien ( 1958 ) for
oogenesis in the ctenostome Alcyonidium diaphanum is also
too general and partly contradicts the phenomenology of the
process. For instance, the early developmental phase was
referred to the as the “period of cytoplasmic growth”, whereas
cytoplasmic volume actually increases during the later “vitellogenesis period”. Hageman ( 1983 ) subdivided the growth
phase into three stages: (a) previtellogenesis, (b) vitellogenesis I, and (c) vitellogenesis II. Combining these approaches,
one can describe oogenesis in Cheilostomata as comprising
three developmental periods, or phases.
1. The initial (previtellogenic) phase begins with division of
the oogonium and the inception of an early previtellogenic doublet consisting of identical cells – the early primary oocytes. In Malacostegina, cytoplasmic bridges
between the siblings are soon destroyed, whereas in
brooding Cheilostomata this pair of cells remains connected while in the ovary. In species with patterns II, III
or IV, a sperm fuses with one of the siblings immediately
or soon after oogonial division, the cells of the doublet
then differentiating into an oocyte and a nurse cell. After
that, the siblings synchronously grow, in preparation for
vitellogenesis. The origin of the follicle/nurse cells in
viviparous Epistomiidae requires further study (see
Sect. 1.2.7 ).
2. The next (vitellogenic) phase begins in Malacostegina
when oocytes are placed in the central growth zone of the
ovary and, in brooding species, into the zone of growth
and ovulation. Such placement results from a general
rearrangement of cells in the ovary both as it grows and
after ovulation. During the vitellogenic phase, nutrient
reserves or their precursors are actively formed and
secreted by ovary cells (both basal cells and wall cells),
being further endocytosed and accumulated in the cytoplasm of the leading oocyte. Additionally, RNA is formed
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
ovary. It is possible, however, that the oocytes of this species
are enlarged mostly through uptake of nutrients from the
coelomic fl uid, as in Membranipora serrilamella (Hageman
1983 ) and Celleporella hyalina (Hughes 1987 ), the oocytes
of which expose part of their microvilli-covered surface to
the coelom remaining embedded in the ovary.
According to the arrangement, structure and size of the
female cells developing in the ovary of brooding cheilostomes, two zones may be delimited: (1) a germinative zone
and (2) a growth-and-ovulation zone. The germinative zone
comprises the basal part of the ovary, i.e. the lower part of the
intraovarian zone limited by the ovary wall of cubic or prismatic cells. It is there that oogonia and previtellogenic doublets occur, most sperm concentrate (and penetrate into the
ovary) and syngamy takes place. Oocytes also increase in
number and undergo the fi rst growth stages there.
The growth-and-ovulation zone comprises the follicle
enveloping the leading oocyte doublet and the uppermost
part of the intraovarian zone directly adjoining the leading
oocyte. This part is represented by a few basal cells and
intercellular spaces between them. The upper and lateral
areas of the follicle wall are composed of fl at (squamous)
cells, while the basal part consists of oval, cubic or prismatic
cells. The main functions of the growth-and-ovulation zone
are the transport of nutrients to the vitellogenic oocyte(s), its
growth accompanied by accumulation of resources, and its
ovulation after maturation.
As the ovary develops and functions, its structure changes
accordingly (see also Dyrynda and King 1983 ). In early ovaries all cells are more or less the same, with differentiation
into wall and basal cells apparently occurring during the
early developmental stages of the fi rst vitellogenic oocyte
and its follicle. The growth of the oocyte is presumably
accompanied by multiplication of ovary cells and changes in
their size and shape; some of the basal and follicle cells
fl atten, whereas the others enlarge and become prismatic or
cuboidal (compare Figs. 1.5A, C and 1.9A, B ). The intraovarian zone gradually fl attens (see Sect. 1.2.4 ).
During and after ovulation, some of the squamous cells of
the follicle apparently degrade. Flat basal cells are no longer
discernible and possibly also degenerate. The follicle walls
“collapse” (see also Vigelius 1882 ) and the intraovarian zone
diminishes considerably. In fact, retention of the ovary during polypide degeneration (sometimes through multiple
recycling) fi ts remarkably well the hypothesis about the
excretory nature of the recycling process (reviewed in
Gordon 1977 ). Contrasting with the adult polypide, which
has no zone of cell proliferation and must degenerate and
regenerate from time to time, oogenetic cycles are accompanied by regular renewal of the cells of the ovary, which may
explain its relative longevity.
There are no essential differences in the structure and function of the ovary in malacostegan and brooding cheilostomes.
In other words, all Cheilostomata have in common a basic
plan of ovarian organization and observed variations
appear to correspond to stages in the evolution of this organ
associated with changes in patterns of oogenesis (see Sect.
3.1.2 ). Any reductions in numbers and size/type of oocytes
would inevitably have resulted in altered gonad structure.
Therefore, one may suggest that differences in ovarian
structure as described above refl ect evolutionary shifts in
oogenesis.
1.3.4 Comparative Analysis of Oogenesis
in Cheilostomata
There are at least three stages in the development of the primary oocyte, from its fi rst appearance to ovulation. A simple
division into previtellogenic and vitellogenic stages (Dyrynda
and King 1983 ) does not quite refl ect the situation. The
descriptive terminology introduced by Chrétien ( 1958 ) for
oogenesis in the ctenostome Alcyonidium diaphanum is also
too general and partly contradicts the phenomenology of the
process. For instance, the early developmental phase was
referred to the as the “period of cytoplasmic growth”, whereas
cytoplasmic volume actually increases during the later “vitellogenesis period”. Hageman ( 1983 ) subdivided the growth
phase into three stages: (a) previtellogenesis, (b) vitellogenesis I, and (c) vitellogenesis II. Combining these approaches,
one can describe oogenesis in Cheilostomata as comprising
three developmental periods, or phases.
1. The initial (previtellogenic) phase begins with division of
the oogonium and the inception of an early previtellogenic doublet consisting of identical cells – the early primary oocytes. In Malacostegina, cytoplasmic bridges
between the siblings are soon destroyed, whereas in
brooding Cheilostomata this pair of cells remains connected while in the ovary. In species with patterns II, III
or IV, a sperm fuses with one of the siblings immediately
or soon after oogonial division, the cells of the doublet
then differentiating into an oocyte and a nurse cell. After
that, the siblings synchronously grow, in preparation for
vitellogenesis. The origin of the follicle/nurse cells in
viviparous Epistomiidae requires further study (see
Sect. 1.2.7 ).
2. The next (vitellogenic) phase begins in Malacostegina
when oocytes are placed in the central growth zone of the
ovary and, in brooding species, into the zone of growth
and ovulation. Such placement results from a general
rearrangement of cells in the ovary both as it grows and
after ovulation. During the vitellogenic phase, nutrient
reserves or their precursors are actively formed and
secreted by ovary cells (both basal cells and wall cells),
being further endocytosed and accumulated in the cytoplasm of the leading oocyte. Additionally, RNA is formed
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis