42
(Ostrovsky 1998 ; Ostrovsky and Schäfer 2003 ; Ostrovsky
et al. 2003 , 2009b ). In some species, brooding occurs
within the so-called internal brood sac – a spacious invagination of the non-calcifi ed wall of the maternal zooid (Figs.
2.6b(E) and 2.7b(C–E) ) (Ostrovsky et al. 2006 , 2007 ,
2009b , c ). In all cases the non- calcifi ed (part of the) wall
that surrounds the incubation space consists of a thin cuticle and the epithelium adjoined by funicular cords and
muscular bundles (see Figs. 1.30B , 1.36B, C , 2.15A, B ,
2.16 , 2.22 , 2.23 , 2.24 , 2.25 , 2.28 , 2.29 , 2.30 , 2.32 , 2.36 ,
2.41 , 2.44 and 2.46 ). Funicular (mesothelial) cells, which
lie on the basal parts of the epithelial cells, are considered
to be part of the somatic peritoneum forming “a reticulate
network … rather than a continuous lining” (Woollacott
and Zimmer 1971 , 1972b , 1975 , p. 359). Thus, epithelial
cells are partially bathed by coelomic fl uid.
In matrotrophic species, the temporary hypertrophy of the
epithelial cells during incubation, along with the increase in
embryo size, provides good evidence that this cell complex
(i.e. the embryophore of epithelial and funicular elements,
see Woollacott and Zimmer 1975 ; Moosbrugger et al. 2012 ;
Ostrovsky 2013 ) is likely to function as the “maternal part”
of the placental analogue. In ovicelled species, the embryophore develops in the wall of the ooecial vesicle (Figs. 1.17B ,
1.18B, G , 1.19B–D , 1.23B , 1.24A , and 1.28C, D ), whereas
in species with brood sacs it develops in much or all of the
sac wall (Fig. 1.23C, D ).
Both zygotes and early embryos surrounded by a fertilization
envelope are suspended in the fl uid of the brood cavity. They
may (Fig. 1.18A ) or may not (Figs. 1.17B , 1.19B, C , 1.23B
and 1.28C ) make contact with the embryophore, even in the
same species. Since embryonic growth results in their
enlargement, they eventually occupy much of or the whole
brood cavity, thus coming into contact with the embryophore
(Figs. 1.18B , 1.19D , 1.23C, D and 1.24A ). Strictly, one may
only speak of the existence of a simple placental analogue
consisting of an embryonic and a maternal part from the
moment the embryo adjoins the embryophore (Ostrovsky
2013 ). Notwithstanding, the embryophore itself is traditionally referred to as the placental analogue [regardless of
whether the growing embryo adjoins it or not].
In Bugula species, the ooecial vesicle of the hyperstomial
ovicell is relatively large, occupying up to half the volume of
brood cavity (Figs. 2.3 and 2.5 ). If the ovicell is empty or
contains a zygote, the epithelial cells of the embryophore are
fl at, and their size is typical of other epithelial cells. When the
ovicell incubates an embryo, the embryophore cells become
active and enlarge drastically (together with their nuclei),
changing their shape from fl at to columnar (Fig. 1.18A, B,
and G ). Cell height varies, but in general it decreases towards
the periphery of the ooecial vesicle. In histological preparations of B . fl abellatа , the basal part (opposite the cuticle of
the vesicle) of these cells is stained more intensely than the
rest of the cytoplasm. A nucleus is positioned in this dark
zone or on the “border” between “pale” and “dark” cytoplasm. The funicular cells of the embryophore (irregular in
shape) are also enlarged, though to a lesser extent. In B . neritina , numerous dark granules can be seen in the funicular
cells and, to a lesser degree, in the hypertrophied epithelial
cells (Fig. 1.18G ), as fi rst described by Woollacott and
Zimmer ( 1972b , 1975 ) (see also Ostrovsky 2013 ).
A similar situation can be observed in the endotoichal
ovicells of Cellaria fi stulosa , where enlarged funicular cells
of the embryophore often form groups, possessing dark
granules in their cytoplasm. During incubation, the entire
cytoplasm of these cells and of the embryophore epithelial
cells is deeply stained, and the latter cells change in shape
from fl at to oval (Fig. 1.19B–D ).
Colonies of Gregarinidra serrata contained only early
embryos, which is why its embryophore cells were not so
prominent and embryo enlargement was not recorded. Even
so, a comparison of the embryophore in the empty and incubating endozooidal ovicells indicates that embryonic brooding is accompanied by a proliferation of epithelial cells
(Fig. 1.17A, B ). The existence of extraembryonic nutrition in
this species is also confi rmed by the considerable difference
between the size of the zygote and early embryo and that of
the brood cavity and by the number, shape and size of the
yolk granules observed in the mature ovarian oocytes and
early embryos. Although not so numerous in the latter, these
granules are considerably larger and likely to adopt a noncircular shape (Fig. 1.17B and inset).
Matrotrophic brooding occurs in internal sacs in
Reciprocus regalis . In this species the brood sac is absent in
hermaphrodite zooids with a feeding polypide, whereas the
ooecial vesicle (homologous to the ooecial vesicle in cheilostomes with ovicells) and its musculature are completely
developed. Beneath the vesicle in the fertile zooid, the noncalcifi ed wall has a small invagination that is obviously an
incipient sac. This structure suggests that the polypide oviposits a small ripe oocyte into it and degenerates soon after.
Eventually the oocyte begins to cleave and the brood sac may
go on to develop in concert with an embryophore and grow
together with the embryo. The absence of the functioning
polypide during incubation indicates that EEN is provisioned
by neighbouring zooids via interzooidal nutrient transport.
Utilization of the polypide remnants (brown body) should be
also possible (see below for details). During incubation, the
cells of embryophore contain small dark granules and sometimes pale vacuoles and their cytoplasm is deeply stained
(Fig. 1.23C, D ).
In many zooids (with or without gonads), very large
vesicular cells (28 μm mean diameter) with “granular” cytoplasm were observed in R. regalis (Fig. 1.23A ). These appear
to be more commonly encountered in incubating zooids and
are often situated near the brood sac or the brown body. One
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
(Ostrovsky 1998 ; Ostrovsky and Schäfer 2003 ; Ostrovsky
et al. 2003 , 2009b ). In some species, brooding occurs
within the so-called internal brood sac – a spacious invagination of the non-calcifi ed wall of the maternal zooid (Figs.
2.6b(E) and 2.7b(C–E) ) (Ostrovsky et al. 2006 , 2007 ,
2009b , c ). In all cases the non- calcifi ed (part of the) wall
that surrounds the incubation space consists of a thin cuticle and the epithelium adjoined by funicular cords and
muscular bundles (see Figs. 1.30B , 1.36B, C , 2.15A, B ,
2.16 , 2.22 , 2.23 , 2.24 , 2.25 , 2.28 , 2.29 , 2.30 , 2.32 , 2.36 ,
2.41 , 2.44 and 2.46 ). Funicular (mesothelial) cells, which
lie on the basal parts of the epithelial cells, are considered
to be part of the somatic peritoneum forming “a reticulate
network … rather than a continuous lining” (Woollacott
and Zimmer 1971 , 1972b , 1975 , p. 359). Thus, epithelial
cells are partially bathed by coelomic fl uid.
In matrotrophic species, the temporary hypertrophy of the
epithelial cells during incubation, along with the increase in
embryo size, provides good evidence that this cell complex
(i.e. the embryophore of epithelial and funicular elements,
see Woollacott and Zimmer 1975 ; Moosbrugger et al. 2012 ;
Ostrovsky 2013 ) is likely to function as the “maternal part”
of the placental analogue. In ovicelled species, the embryophore develops in the wall of the ooecial vesicle (Figs. 1.17B ,
1.18B, G , 1.19B–D , 1.23B , 1.24A , and 1.28C, D ), whereas
in species with brood sacs it develops in much or all of the
sac wall (Fig. 1.23C, D ).
Both zygotes and early embryos surrounded by a fertilization
envelope are suspended in the fl uid of the brood cavity. They
may (Fig. 1.18A ) or may not (Figs. 1.17B , 1.19B, C , 1.23B
and 1.28C ) make contact with the embryophore, even in the
same species. Since embryonic growth results in their
enlargement, they eventually occupy much of or the whole
brood cavity, thus coming into contact with the embryophore
(Figs. 1.18B , 1.19D , 1.23C, D and 1.24A ). Strictly, one may
only speak of the existence of a simple placental analogue
consisting of an embryonic and a maternal part from the
moment the embryo adjoins the embryophore (Ostrovsky
2013 ). Notwithstanding, the embryophore itself is traditionally referred to as the placental analogue [regardless of
whether the growing embryo adjoins it or not].
In Bugula species, the ooecial vesicle of the hyperstomial
ovicell is relatively large, occupying up to half the volume of
brood cavity (Figs. 2.3 and 2.5 ). If the ovicell is empty or
contains a zygote, the epithelial cells of the embryophore are
fl at, and their size is typical of other epithelial cells. When the
ovicell incubates an embryo, the embryophore cells become
active and enlarge drastically (together with their nuclei),
changing their shape from fl at to columnar (Fig. 1.18A, B,
and G ). Cell height varies, but in general it decreases towards
the periphery of the ooecial vesicle. In histological preparations of B . fl abellatа , the basal part (opposite the cuticle of
the vesicle) of these cells is stained more intensely than the
rest of the cytoplasm. A nucleus is positioned in this dark
zone or on the “border” between “pale” and “dark” cytoplasm. The funicular cells of the embryophore (irregular in
shape) are also enlarged, though to a lesser extent. In B . neritina , numerous dark granules can be seen in the funicular
cells and, to a lesser degree, in the hypertrophied epithelial
cells (Fig. 1.18G ), as fi rst described by Woollacott and
Zimmer ( 1972b , 1975 ) (see also Ostrovsky 2013 ).
A similar situation can be observed in the endotoichal
ovicells of Cellaria fi stulosa , where enlarged funicular cells
of the embryophore often form groups, possessing dark
granules in their cytoplasm. During incubation, the entire
cytoplasm of these cells and of the embryophore epithelial
cells is deeply stained, and the latter cells change in shape
from fl at to oval (Fig. 1.19B–D ).
Colonies of Gregarinidra serrata contained only early
embryos, which is why its embryophore cells were not so
prominent and embryo enlargement was not recorded. Even
so, a comparison of the embryophore in the empty and incubating endozooidal ovicells indicates that embryonic brooding is accompanied by a proliferation of epithelial cells
(Fig. 1.17A, B ). The existence of extraembryonic nutrition in
this species is also confi rmed by the considerable difference
between the size of the zygote and early embryo and that of
the brood cavity and by the number, shape and size of the
yolk granules observed in the mature ovarian oocytes and
early embryos. Although not so numerous in the latter, these
granules are considerably larger and likely to adopt a noncircular shape (Fig. 1.17B and inset).
Matrotrophic brooding occurs in internal sacs in
Reciprocus regalis . In this species the brood sac is absent in
hermaphrodite zooids with a feeding polypide, whereas the
ooecial vesicle (homologous to the ooecial vesicle in cheilostomes with ovicells) and its musculature are completely
developed. Beneath the vesicle in the fertile zooid, the noncalcifi ed wall has a small invagination that is obviously an
incipient sac. This structure suggests that the polypide oviposits a small ripe oocyte into it and degenerates soon after.
Eventually the oocyte begins to cleave and the brood sac may
go on to develop in concert with an embryophore and grow
together with the embryo. The absence of the functioning
polypide during incubation indicates that EEN is provisioned
by neighbouring zooids via interzooidal nutrient transport.
Utilization of the polypide remnants (brown body) should be
also possible (see below for details). During incubation, the
cells of embryophore contain small dark granules and sometimes pale vacuoles and their cytoplasm is deeply stained
(Fig. 1.23C, D ).
In many zooids (with or without gonads), very large
vesicular cells (28 μm mean diameter) with “granular” cytoplasm were observed in R. regalis (Fig. 1.23A ). These appear
to be more commonly encountered in incubating zooids and
are often situated near the brood sac or the brown body. One
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis