17
wall of the cystid and in two other species, on the distal
transverse walls (Fig. 1.18F ). In Cauloramphus spinifer the
ovary sometimes occupies the corner between the proximal
transverse wall and the frontal wall of the cystid.
In general, the position of the ovary is quite stable within a
species. For example, in Callopora lineata the ovary was
always located in the distal half of the fertile zooid, almost
invariably lying on its basal wall (Figs. 1.4 , 1.5 and 1.6C, D ).
On the other hand, in Bugula fl abellata , the ovary may be situated in the middle part of the zooid or distally, either on the
basal wall (Fig. 1.18C, D ) or suspended on funicular cords.
Within a genus, the position of the ovary is the same or
similar in different species. There are, however, several
exceptions. In the fl ustrids Gregarinidra inarmata and
Isosecurifl ustra tenuis , the ovary lies on the basal wall in the
proximal part of the zooid, while in G . serrata and I . angusta
it is distal. In Callopora lineata , C . craticula and
Schizomavella lineata the ovary is located in the distal half
of the zooid, while in C . dumerilii and S . cuspidata it is proximal. Within families the position of the ovary can be more
variable. The family Candidae is in general characterized by
a distal position for the ovary (seven genera studied) but one
exception was encountered ( Bugulopsis monotrypa ) with a
proximal position. Among calloporids, the ovary is located
proximally or in the middle part of the zooid in three genera
( Callopora , Cauloramphus , Crassimarginatella ) and in the
middle or distally in four genera ( Bryocalyx , Callopora ,
Tegella , Valdemunitella ). In the Bugulidae the ovary may be
located distally ( Bugula , Dendrobeania ), proximally
( Cornucopina ) or in the middle ( Dimetopia ) (Table 1.1 ).
In several respects my results are in excellent agreement
with those of Calvet ( 1900 ); the position of the ovary is generally constant within a species but may vary in some cases; the
ovary lies on the basal wall in most species but in some may be
suspended on funicular cords in the zooidal cavity. In several
cases I found both instances in the same species (Table 1.1 ).
An ovary associated with the polypide has been found in some
zooids of Bicellariella ciliata only. Also in this species two
early doublets of female cells (presumably oogonia), located
far from each other, were recorded in one young polypide bud
(Moosbrugger et al. 2012 ). This fi nding supports a report of
Calvet ( 1900 ) about two ovaries in a single zooid of Bugula
simplex . Reports of several ovaries in zooids of Einhornia
crustulenta (Schulz 1901 ; Borg 1947 ) require verifi cation.
1.2.3 Reproductive Pattern I
in Cheilostomata
The oldest (least-derived, therefore inferred fi rst-appearing)
pattern of sexual reproduction in cheilostomes is characterized
by the simultaneous or near-simultaneous formation in the
ovary of numerous (sometimes, several) small oligolecithal
oocytes (100 μm or less) that, after maturation, ovulation and
spawning, develop into planktotrophic larvae (cyphonautes
larvae). Fertilization is intracoelomic and occurs at or near
ovulation. Karyogamy is delayed and occurs after spawning
of oocytes via intertentacular organ. There is no brooding.
This broadcasting pattern is characteristic only of cheilostomes in suborder Malacostegina (Figs. 1.1 , 1.2 and 1.3 ).
1.2.3.1 Ovary Structure and Oogenesis
in Membranipora serrilamella
and Electra pilosa
The most detailed source of information on oogenesis in
Malacostegina is the unpublished dissertation of Hageman
( 1983 ), who studied Membranipora serrilamella using both
light and transmission electron microscopy.
In this species the ovary differentiates in zooids with a
functional polypide. It is fi rst apparent within the parietal
peritoneum on one of the lateral walls in the proximal part of
the zooid, at the site where several funicular strands fuse.
Ovaries of adjacent zooids are often located close to each
other, adjoining the same pore plate from different sides.
Developing somatic peritoneum forms follicle epithelium
around oogonia and oocytes. Between the ovary and the
epidermal cells of the cystid wall a so-called “subovarian
space” is formed, consisting of one to two layers of peritoneally derived “basal cells” and an intercellular “interstitial
space” into which the lacunae of the ingoing funicular cords
open; these have a transport function. Follicle cells are
involved in regulating vitellogenesis, controlling access of
oocytes to the subovarian space, synchronizing differentiation of oocytes and transporting towards them low-molecular
metabolites including yolk precursors. Follicle cells also
phagocytose degrading oocytes.
The fully functioning ovary consists of three zones: (1) a
peripheral germinal zone, (2) a central growth zone, and (3) a
centro-apical ovulatory zone. In the germinal zone follicle
cells surround oogonia and early previtellogenic oocytes.
Oogonia divide there, resulting in primary oocytes 5 μm in
diameter, which for some time remain connected by cytoplasmic bridges. In the central growth zone the follicle epithelium
is incomplete basally, and developing oocytes at various
stages of vitellogenesis are in contact with the subovarian
space: the lower surface of the oocytes faces the slit- like
lumen between them and basal cells. In the basal cells and
oocytes the number of organelles involved in the synthesis of
reserve nutrients (including rough endoplasmatic reticulum)
increases greatly. The subovarian space is enlarged and its
lacunae are fi lled with a proteinase substance secreted by the
basal cells and some funicular-cord cells. This substance is
endocytosed by growing oocytes, its components being incorporated into the yolk granules that form in the ooplasm. Thus,
ultrastructural observations indicate that yolk originates from
the basal cells as well as from the oocyte itself.
1.2 Reproductive Patterns of Bryozoa
wall of the cystid and in two other species, on the distal
transverse walls (Fig. 1.18F ). In Cauloramphus spinifer the
ovary sometimes occupies the corner between the proximal
transverse wall and the frontal wall of the cystid.
In general, the position of the ovary is quite stable within a
species. For example, in Callopora lineata the ovary was
always located in the distal half of the fertile zooid, almost
invariably lying on its basal wall (Figs. 1.4 , 1.5 and 1.6C, D ).
On the other hand, in Bugula fl abellata , the ovary may be situated in the middle part of the zooid or distally, either on the
basal wall (Fig. 1.18C, D ) or suspended on funicular cords.
Within a genus, the position of the ovary is the same or
similar in different species. There are, however, several
exceptions. In the fl ustrids Gregarinidra inarmata and
Isosecurifl ustra tenuis , the ovary lies on the basal wall in the
proximal part of the zooid, while in G . serrata and I . angusta
it is distal. In Callopora lineata , C . craticula and
Schizomavella lineata the ovary is located in the distal half
of the zooid, while in C . dumerilii and S . cuspidata it is proximal. Within families the position of the ovary can be more
variable. The family Candidae is in general characterized by
a distal position for the ovary (seven genera studied) but one
exception was encountered ( Bugulopsis monotrypa ) with a
proximal position. Among calloporids, the ovary is located
proximally or in the middle part of the zooid in three genera
( Callopora , Cauloramphus , Crassimarginatella ) and in the
middle or distally in four genera ( Bryocalyx , Callopora ,
Tegella , Valdemunitella ). In the Bugulidae the ovary may be
located distally ( Bugula , Dendrobeania ), proximally
( Cornucopina ) or in the middle ( Dimetopia ) (Table 1.1 ).
In several respects my results are in excellent agreement
with those of Calvet ( 1900 ); the position of the ovary is generally constant within a species but may vary in some cases; the
ovary lies on the basal wall in most species but in some may be
suspended on funicular cords in the zooidal cavity. In several
cases I found both instances in the same species (Table 1.1 ).
An ovary associated with the polypide has been found in some
zooids of Bicellariella ciliata only. Also in this species two
early doublets of female cells (presumably oogonia), located
far from each other, were recorded in one young polypide bud
(Moosbrugger et al. 2012 ). This fi nding supports a report of
Calvet ( 1900 ) about two ovaries in a single zooid of Bugula
simplex . Reports of several ovaries in zooids of Einhornia
crustulenta (Schulz 1901 ; Borg 1947 ) require verifi cation.
1.2.3 Reproductive Pattern I
in Cheilostomata
The oldest (least-derived, therefore inferred fi rst-appearing)
pattern of sexual reproduction in cheilostomes is characterized
by the simultaneous or near-simultaneous formation in the
ovary of numerous (sometimes, several) small oligolecithal
oocytes (100 μm or less) that, after maturation, ovulation and
spawning, develop into planktotrophic larvae (cyphonautes
larvae). Fertilization is intracoelomic and occurs at or near
ovulation. Karyogamy is delayed and occurs after spawning
of oocytes via intertentacular organ. There is no brooding.
This broadcasting pattern is characteristic only of cheilostomes in suborder Malacostegina (Figs. 1.1 , 1.2 and 1.3 ).
1.2.3.1 Ovary Structure and Oogenesis
in Membranipora serrilamella
and Electra pilosa
The most detailed source of information on oogenesis in
Malacostegina is the unpublished dissertation of Hageman
( 1983 ), who studied Membranipora serrilamella using both
light and transmission electron microscopy.
In this species the ovary differentiates in zooids with a
functional polypide. It is fi rst apparent within the parietal
peritoneum on one of the lateral walls in the proximal part of
the zooid, at the site where several funicular strands fuse.
Ovaries of adjacent zooids are often located close to each
other, adjoining the same pore plate from different sides.
Developing somatic peritoneum forms follicle epithelium
around oogonia and oocytes. Between the ovary and the
epidermal cells of the cystid wall a so-called “subovarian
space” is formed, consisting of one to two layers of peritoneally derived “basal cells” and an intercellular “interstitial
space” into which the lacunae of the ingoing funicular cords
open; these have a transport function. Follicle cells are
involved in regulating vitellogenesis, controlling access of
oocytes to the subovarian space, synchronizing differentiation of oocytes and transporting towards them low-molecular
metabolites including yolk precursors. Follicle cells also
phagocytose degrading oocytes.
The fully functioning ovary consists of three zones: (1) a
peripheral germinal zone, (2) a central growth zone, and (3) a
centro-apical ovulatory zone. In the germinal zone follicle
cells surround oogonia and early previtellogenic oocytes.
Oogonia divide there, resulting in primary oocytes 5 μm in
diameter, which for some time remain connected by cytoplasmic bridges. In the central growth zone the follicle epithelium
is incomplete basally, and developing oocytes at various
stages of vitellogenesis are in contact with the subovarian
space: the lower surface of the oocytes faces the slit- like
lumen between them and basal cells. In the basal cells and
oocytes the number of organelles involved in the synthesis of
reserve nutrients (including rough endoplasmatic reticulum)
increases greatly. The subovarian space is enlarged and its
lacunae are fi lled with a proteinase substance secreted by the
basal cells and some funicular-cord cells. This substance is
endocytosed by growing oocytes, its components being incorporated into the yolk granules that form in the ooplasm. Thus,
ultrastructural observations indicate that yolk originates from
the basal cells as well as from the oocyte itself.
1.2 Reproductive Patterns of Bryozoa