46
contains large pale vacuoles (Fig. 1.21A ). Sacs with late
embryos and larvae have only pale vacuoles in these cells,
which became more fl attened (Fig. 1.21B ). After larval
release, embryophore cells lose most of their inclusions. A
well-developed embryophore of cuboidal epithelial cells
covered by the funicular cells occurs in Bicellariella ciliata
(Moosbrugger et al. 2012 ).
The embryophore and funicular system are highly developed in Costaticella solida (Fig. 1.25 ). During incubation,
the cytoplasm of the hypertrophied epithelial cells contains
pale vacuoles and small dark granules that are also observed
in associated funicular cells of irregular shape. Both epithelial and funicular cells stain intensely, but the cytoplasm of
the former is much darker. Compared with most of the species studied, funicular cells of Costaticella solida form a
loose “tissue” that almost completely covers the basal parts
of epithelial cells (Fig. 1.25B ). This “tissue” is continuous
with a dense reticulate network of funicular cords that course
towards the proximal zooid wall, undergoing a gradual
decrease in cell size and containing a smaller number of
cytoplasmic granules. Numerous groups of collapsing cells
of a yellowish-green colour (presumed to be remnants of the
brown body) were detected between and inside funicular
cords. Granules of the same colouration were also found in
the intercellular spaces between epithelial and funicular cells
of the embryophore and possibly also in their cytoplasm.
Putative “nutrient storage cells”, large and oval with a pale
vesicular nucleus and dark fi ne-grained cytoplasm, are commonly found between strands of the funicular network and
on the zooid wall.
In Costaticella bicuspis , the embryophore consists of
relatively small, oval, densely packed epithelial cells with
dark cytoplasm and a 2–3-layered complex of paler, large,
oval or irregular funicular cells that make up the funicular
“tissue” (see above). As in C. solida , this cellular complex is
connected to a system of funicular cords, most of which
form a compact central “trunk” that continues to the proximal zooid. In one of the zooids the funicular tissue of the
embryophore was seen to have been invaded by fungal
hyphae (Fig. 1.24B ).
In the hyperstomial ovicells of “Calyptotheca” variolosa ,
the fl at epithelial cells of the embryophore become large and
columnar, with pale cytoplasm and darker nuclei (Fig. 1.33C ).
Small dark granules (not very numerous) become visible in
embryophore cells at early growth stages and continue to be
seen throughout fi rst part of the brooding period (Fig. 1.33B, E ).
Numerous tiny granules were noted in the cytoplasm of
embryophore cells in the internal brood sac in Watersipora
subtorquata .
Finally, Myriapora truncata has a well-developed
embryophore consisting of cubic and columnar epithelial
cells with intensely staining cytoplasm and numerous pale
vacuoles (Fig. 1.33A ). The funicular cells form a reticulate
network inside the ooecial vesicle of the endozooidal
ovicells.
There is a possibility that extraembryonic nutrition may
also exist in Scrupocellaria scruposa (see Ostrovsky et al.
2009a ), but additional research will be needed to confi rm
this. The epithelial cells of the ooecial vesicle in the hyperstomial ovicell in this species are no larger than other bodywall cells, but the formation of a more-or-less complete layer
and intense staining during embryo incubation could be a
sign of increased physiological activity. Extraembryonic
nutrition in this genus was discovered by Santagata and
Banta ( 1996 ). They reported a doubling in size of the embryo
in S . ferox (with reproductive pattern IV), which agrees well
with my data (1.8-fold) for S. scruposa . In fact, my recalculation of the data given for S. ferox by Santagata and Banta
( 1996 ) yields an almost fi ve-fold increase.
Taking into account the degree of embryophore-cell
hypertrophy and embryo enlargement during incubation, and
the relation between the size of the mature oocyte and that of
the brood cavity, species with pattern IV may be classifi ed
into four categories:
1. Species with a small embryophore and negligible or little
(less than 1.5-fold) embryo enlargement ( Klugefl ustra
antarctica , Isosecurifl ustra angusta , Micropora notialis ,
Figularia fi gularis ). Mature oocytes are slightly smaller
than the brood cavity or comparable to it.
2. Species with modest hypertrophy of embryophore cells,
but a functionally active embryophore and considerable
embryonic enlargement (three-fold and more) ( Cellaria
tenuirostris , Cribricellina cribraria , Watersipora subtorquata ). Mature oocytes are smaller than the brood
cavity.
3. Species with a well-developed embryophore of strongly
hypertrophied cells and embryo enlargement from considerable (4.9-fold) to very substantial (468.2-fold).
Mature oocytes are somewhat or very much smaller than
the brood cavity ( Beania bilaminata , Celleporella hyalina , Bicellariella ciliata, “Calyptotheca” variolosa ,
Costaticella solida , C . bicuspis ). Beania bilaminata is a
special case, having the second-largest embryo enlargement recorded in cheilostomes ( Bugula neritina has the
largest, at 500-fold; see Woollacott and Zimmer 1975 ).
4. Species with a well-developed embryophore and apparently
negligible embryo enlargement ( Myriapora truncata ).
The varied degrees of development among placental analogues in species with reproductive pattern IV may refl ect
the evolutionary transition towards more effective extraembryonic nutrition (Ostrovsky 2013 ). If so, a weakly
developed embryophore is consistent with having a large
oocyte (see, for instance, Fig. 1.32B, C ). At the same time,
it remains unclear why Myriapora truncata , with large
oocytes completely occupying the brood cavity, develops a
large embryophore (Fig. 1.33A ), especially since small
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
contains large pale vacuoles (Fig. 1.21A ). Sacs with late
embryos and larvae have only pale vacuoles in these cells,
which became more fl attened (Fig. 1.21B ). After larval
release, embryophore cells lose most of their inclusions. A
well-developed embryophore of cuboidal epithelial cells
covered by the funicular cells occurs in Bicellariella ciliata
(Moosbrugger et al. 2012 ).
The embryophore and funicular system are highly developed in Costaticella solida (Fig. 1.25 ). During incubation,
the cytoplasm of the hypertrophied epithelial cells contains
pale vacuoles and small dark granules that are also observed
in associated funicular cells of irregular shape. Both epithelial and funicular cells stain intensely, but the cytoplasm of
the former is much darker. Compared with most of the species studied, funicular cells of Costaticella solida form a
loose “tissue” that almost completely covers the basal parts
of epithelial cells (Fig. 1.25B ). This “tissue” is continuous
with a dense reticulate network of funicular cords that course
towards the proximal zooid wall, undergoing a gradual
decrease in cell size and containing a smaller number of
cytoplasmic granules. Numerous groups of collapsing cells
of a yellowish-green colour (presumed to be remnants of the
brown body) were detected between and inside funicular
cords. Granules of the same colouration were also found in
the intercellular spaces between epithelial and funicular cells
of the embryophore and possibly also in their cytoplasm.
Putative “nutrient storage cells”, large and oval with a pale
vesicular nucleus and dark fi ne-grained cytoplasm, are commonly found between strands of the funicular network and
on the zooid wall.
In Costaticella bicuspis , the embryophore consists of
relatively small, oval, densely packed epithelial cells with
dark cytoplasm and a 2–3-layered complex of paler, large,
oval or irregular funicular cells that make up the funicular
“tissue” (see above). As in C. solida , this cellular complex is
connected to a system of funicular cords, most of which
form a compact central “trunk” that continues to the proximal zooid. In one of the zooids the funicular tissue of the
embryophore was seen to have been invaded by fungal
hyphae (Fig. 1.24B ).
In the hyperstomial ovicells of “Calyptotheca” variolosa ,
the fl at epithelial cells of the embryophore become large and
columnar, with pale cytoplasm and darker nuclei (Fig. 1.33C ).
Small dark granules (not very numerous) become visible in
embryophore cells at early growth stages and continue to be
seen throughout fi rst part of the brooding period (Fig. 1.33B, E ).
Numerous tiny granules were noted in the cytoplasm of
embryophore cells in the internal brood sac in Watersipora
subtorquata .
Finally, Myriapora truncata has a well-developed
embryophore consisting of cubic and columnar epithelial
cells with intensely staining cytoplasm and numerous pale
vacuoles (Fig. 1.33A ). The funicular cells form a reticulate
network inside the ooecial vesicle of the endozooidal
ovicells.
There is a possibility that extraembryonic nutrition may
also exist in Scrupocellaria scruposa (see Ostrovsky et al.
2009a ), but additional research will be needed to confi rm
this. The epithelial cells of the ooecial vesicle in the hyperstomial ovicell in this species are no larger than other bodywall cells, but the formation of a more-or-less complete layer
and intense staining during embryo incubation could be a
sign of increased physiological activity. Extraembryonic
nutrition in this genus was discovered by Santagata and
Banta ( 1996 ). They reported a doubling in size of the embryo
in S . ferox (with reproductive pattern IV), which agrees well
with my data (1.8-fold) for S. scruposa . In fact, my recalculation of the data given for S. ferox by Santagata and Banta
( 1996 ) yields an almost fi ve-fold increase.
Taking into account the degree of embryophore-cell
hypertrophy and embryo enlargement during incubation, and
the relation between the size of the mature oocyte and that of
the brood cavity, species with pattern IV may be classifi ed
into four categories:
1. Species with a small embryophore and negligible or little
(less than 1.5-fold) embryo enlargement ( Klugefl ustra
antarctica , Isosecurifl ustra angusta , Micropora notialis ,
Figularia fi gularis ). Mature oocytes are slightly smaller
than the brood cavity or comparable to it.
2. Species with modest hypertrophy of embryophore cells,
but a functionally active embryophore and considerable
embryonic enlargement (three-fold and more) ( Cellaria
tenuirostris , Cribricellina cribraria , Watersipora subtorquata ). Mature oocytes are smaller than the brood
cavity.
3. Species with a well-developed embryophore of strongly
hypertrophied cells and embryo enlargement from considerable (4.9-fold) to very substantial (468.2-fold).
Mature oocytes are somewhat or very much smaller than
the brood cavity ( Beania bilaminata , Celleporella hyalina , Bicellariella ciliata, “Calyptotheca” variolosa ,
Costaticella solida , C . bicuspis ). Beania bilaminata is a
special case, having the second-largest embryo enlargement recorded in cheilostomes ( Bugula neritina has the
largest, at 500-fold; see Woollacott and Zimmer 1975 ).
4. Species with a well-developed embryophore and apparently
negligible embryo enlargement ( Myriapora truncata ).
The varied degrees of development among placental analogues in species with reproductive pattern IV may refl ect
the evolutionary transition towards more effective extraembryonic nutrition (Ostrovsky 2013 ). If so, a weakly
developed embryophore is consistent with having a large
oocyte (see, for instance, Fig. 1.32B, C ). At the same time,
it remains unclear why Myriapora truncata , with large
oocytes completely occupying the brood cavity, develops a
large embryophore (Fig. 1.33A ), especially since small
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis