54
by means of intracolonial transport from neighbouring
zooids through interzooidal pores via the funicular system.
The same “continuity” is characteristic of matrotrophic incubation in specialized zooids with regressed polypides in
viviparous bryozoans of the order Cyclostomata, as well as
in epistomiids and brooding ctenostomes and cheilostomes
with EEN. Interzooidal transport allows for uninterrupted
nutrient supply to gonads and embryos in non-feeding
zooids, thus sustaining appropriate reproduction rates.
Marcus ( 1941a ) wrote that in Thalamoporella evelinae
the cells of the “peduncle” [basal part] of the ovary enlarged
and became fi lled with “yolk granules” at the onset of vitellogenesis. The lumen of the peduncle [intraovarian zone]
became fi lled with the same material. The secretion of proteinase in the lumen of the intraovarian zone is suggested in
Securifl ustra securifrons and Isosecurifl ustra tenuis . In my
material, lacunar fl uid stains intensely in histological sections in these species. This suggests that the cells of the
lumen [presumably basal cells] are involved in the synthesis
and transport of nutrients for the growing oocyte. Although
Marcus worked at the level of light microscopy, the sequence
of events described by him was essentially correct, as demonstrated by Hageman ( 1983 ) using Tem in Membranipora
serrilamella . Therefore, it is possible that nutrient transfer
by exocytosis from the basal cells into the lacunae of the
intraovarian space and thence by endocytosis into the growing oocytes is a universal mechanism in cheilostomes. For
example, in Chartella papyracea Dyrynda and King ( 1983 )
found that protein (yolk) granules appeared in the cytoplasm
of the oocyte during early and middle vitellogenic stages.
The oocyte formed microvilli, between the bases of which
pinocytotic vacuoles were found. The same processes,
including pinocytosis, occur in the nurse cell that also
produces and transports ribosomes to its sibling via a cytoplasmic bridge. The epithelium of the ovary wall also shows
signs of synthesis and transport activity. Thus, the funicular
system, cells of the ovary and the nurse cell provide the
reserves that are accumulated in the vitellogenic oocyte. An
important aspect in the formation of nutrients seems to be
that of autosynthesis in the oocyte itself (see Reed 1991 ),
whose enhanced activity is evidenced by a large nucleolus
(sometimes several) and, in some species, lobate nuclei.
My histological data confi rm the enhanced activity of
ovary-wall cells, which, as a rule, increase in size and
number and stain intensely (except for the fl at follicle cells
and basal cells) if the gonad contains a vitellogenic oocyte.
In Cornucopina polymorpha , the dark-staining cells of the
ovary wall contain large pale vacuoles often arranged in a
longitudinal row along the basal-apical axis of the cell
(Fig. 1.11B ). Pale vacuoles and the very tiny granules were
noted in prismatic ovary-wall cells in Cribrilina annulata
(Fig. 1.10C, D ). Conspicuous dark granules were found in
basal cells (including fl attened ones) in Arctonula arctica .
In “Calyptotheca” variolosa , the cytoplasm of many
ovary- wall cells, including fl at follicle cells, contained small
dark granules (Fig. 1.33F ). So far this is the only indication
that squamous follicle cells may be involved in vitellogenesis or at least in the transport of nutrients. In contrast, follicle
cells contain no granules in ovaries with an early vitellogenic doublet in this species. Hughes ( 1987 ), using ТЕМ,
demonstrated in Celleporella hyalina the presence of small
vesicles in the follicle cells; these resemble the granular
material in the oocyte as seen by TEM. Signs of enhanced
synthesis were also found in the outer columnar layer of
the ovary wall in Chartella papyracea (see Dyrynda and
King 1983 ). Given that the structure of the ovary is similar
in cheilostome bryozoans (see Sect. 1.2 ) with different
reproductive patterns, it may be suggested that similar
mechanisms for accumulating resources in oocytes are to be
found throughout this order.
The discovery of irregular outgrowths on the lower surface of vitellogenic oocytes exposed to the intraovarian space
in Nematofl ustra fl agellata may indicate the existence of yet
another mechanism. In sections, it appears that these outgrowths are formed by fusion of the basal cells of the intraovarian zone with the oocyte (Fig. 1.12C ). If this is so, it may
mean that the basal cells are either phagocytosed by the
oocyte or form cytoplasmic bridges for the transfer of substances and organelles.
In addition to the above-described method of absorption
of substances by the oocyte from the “central channel” in
Thalamoporella evelinae , Marcus ( 1941a ) suggested that
the partly ovulated oocyte could be nourished by a special
area of peritoneum of the frontal wall of the cystid, consisting of large columnar cells. These cells contain numerous
“yolk” granules; their apical areas, which are brush-like
(probably microvillar), are appressed to the oocyte. Marcus
also found on the walls of the brooding zooid large cells that
are presumably involved in the accumulation and storage of
nutrient reserves.
The vegetal pole of the mature oocyte in most cases
adjoins the intraovarian zone, while the animal pole is surrounded by fl attened follicle cells (Figs. 1.5C , 1.6C , 1.9B ,
1.10D , 1.14C , 1.27A , 1.30A and 1.33F ). If we assume that
most nutrients are supplied to the female cell from the side of
the intraovarian zone, the position of the nucleus may be a
consequence of the numerous yolk granules accumulating at
the vegetal pole gradually forcing the nucleus back to the
opposite part of the cell.
1.3.4.2 Nurse Cells
Nurse cells are mitotic twins of oocytes. During oogenesis a
nurse cell participates in oocyte development, being connected to it by a cytoplasmic bridge. Nurse cells evolved
independently in several invertebrate groups, including
coelenterates, ctenophores, annelids, chitons, priapulids,
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
by means of intracolonial transport from neighbouring
zooids through interzooidal pores via the funicular system.
The same “continuity” is characteristic of matrotrophic incubation in specialized zooids with regressed polypides in
viviparous bryozoans of the order Cyclostomata, as well as
in epistomiids and brooding ctenostomes and cheilostomes
with EEN. Interzooidal transport allows for uninterrupted
nutrient supply to gonads and embryos in non-feeding
zooids, thus sustaining appropriate reproduction rates.
Marcus ( 1941a ) wrote that in Thalamoporella evelinae
the cells of the “peduncle” [basal part] of the ovary enlarged
and became fi lled with “yolk granules” at the onset of vitellogenesis. The lumen of the peduncle [intraovarian zone]
became fi lled with the same material. The secretion of proteinase in the lumen of the intraovarian zone is suggested in
Securifl ustra securifrons and Isosecurifl ustra tenuis . In my
material, lacunar fl uid stains intensely in histological sections in these species. This suggests that the cells of the
lumen [presumably basal cells] are involved in the synthesis
and transport of nutrients for the growing oocyte. Although
Marcus worked at the level of light microscopy, the sequence
of events described by him was essentially correct, as demonstrated by Hageman ( 1983 ) using Tem in Membranipora
serrilamella . Therefore, it is possible that nutrient transfer
by exocytosis from the basal cells into the lacunae of the
intraovarian space and thence by endocytosis into the growing oocytes is a universal mechanism in cheilostomes. For
example, in Chartella papyracea Dyrynda and King ( 1983 )
found that protein (yolk) granules appeared in the cytoplasm
of the oocyte during early and middle vitellogenic stages.
The oocyte formed microvilli, between the bases of which
pinocytotic vacuoles were found. The same processes,
including pinocytosis, occur in the nurse cell that also
produces and transports ribosomes to its sibling via a cytoplasmic bridge. The epithelium of the ovary wall also shows
signs of synthesis and transport activity. Thus, the funicular
system, cells of the ovary and the nurse cell provide the
reserves that are accumulated in the vitellogenic oocyte. An
important aspect in the formation of nutrients seems to be
that of autosynthesis in the oocyte itself (see Reed 1991 ),
whose enhanced activity is evidenced by a large nucleolus
(sometimes several) and, in some species, lobate nuclei.
My histological data confi rm the enhanced activity of
ovary-wall cells, which, as a rule, increase in size and
number and stain intensely (except for the fl at follicle cells
and basal cells) if the gonad contains a vitellogenic oocyte.
In Cornucopina polymorpha , the dark-staining cells of the
ovary wall contain large pale vacuoles often arranged in a
longitudinal row along the basal-apical axis of the cell
(Fig. 1.11B ). Pale vacuoles and the very tiny granules were
noted in prismatic ovary-wall cells in Cribrilina annulata
(Fig. 1.10C, D ). Conspicuous dark granules were found in
basal cells (including fl attened ones) in Arctonula arctica .
In “Calyptotheca” variolosa , the cytoplasm of many
ovary- wall cells, including fl at follicle cells, contained small
dark granules (Fig. 1.33F ). So far this is the only indication
that squamous follicle cells may be involved in vitellogenesis or at least in the transport of nutrients. In contrast, follicle
cells contain no granules in ovaries with an early vitellogenic doublet in this species. Hughes ( 1987 ), using ТЕМ,
demonstrated in Celleporella hyalina the presence of small
vesicles in the follicle cells; these resemble the granular
material in the oocyte as seen by TEM. Signs of enhanced
synthesis were also found in the outer columnar layer of
the ovary wall in Chartella papyracea (see Dyrynda and
King 1983 ). Given that the structure of the ovary is similar
in cheilostome bryozoans (see Sect. 1.2 ) with different
reproductive patterns, it may be suggested that similar
mechanisms for accumulating resources in oocytes are to be
found throughout this order.
The discovery of irregular outgrowths on the lower surface of vitellogenic oocytes exposed to the intraovarian space
in Nematofl ustra fl agellata may indicate the existence of yet
another mechanism. In sections, it appears that these outgrowths are formed by fusion of the basal cells of the intraovarian zone with the oocyte (Fig. 1.12C ). If this is so, it may
mean that the basal cells are either phagocytosed by the
oocyte or form cytoplasmic bridges for the transfer of substances and organelles.
In addition to the above-described method of absorption
of substances by the oocyte from the “central channel” in
Thalamoporella evelinae , Marcus ( 1941a ) suggested that
the partly ovulated oocyte could be nourished by a special
area of peritoneum of the frontal wall of the cystid, consisting of large columnar cells. These cells contain numerous
“yolk” granules; their apical areas, which are brush-like
(probably microvillar), are appressed to the oocyte. Marcus
also found on the walls of the brooding zooid large cells that
are presumably involved in the accumulation and storage of
nutrient reserves.
The vegetal pole of the mature oocyte in most cases
adjoins the intraovarian zone, while the animal pole is surrounded by fl attened follicle cells (Figs. 1.5C , 1.6C , 1.9B ,
1.10D , 1.14C , 1.27A , 1.30A and 1.33F ). If we assume that
most nutrients are supplied to the female cell from the side of
the intraovarian zone, the position of the nucleus may be a
consequence of the numerous yolk granules accumulating at
the vegetal pole gradually forcing the nucleus back to the
opposite part of the cell.
1.3.4.2 Nurse Cells
Nurse cells are mitotic twins of oocytes. During oogenesis a
nurse cell participates in oocyte development, being connected to it by a cytoplasmic bridge. Nurse cells evolved
independently in several invertebrate groups, including
coelenterates, ctenophores, annelids, chitons, priapulids,
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis