43
potential hypothesis is that these cells function as “nutrient
storage cells”. Such cells, round or oval and ca. 8–15 μm
diameter, were fi rst described in Bugula fl abellatа by
Dyrynda and King ( 1983 , p. 487). They were found to be
abundant throughout the cystid in my material too
(Fig. 1.18E ), often associated with funicular cords where
they were in contact with the zooid wall. They stain deeply
and sometimes contain large pale vacuoles, also illustrated
by Dyrynda and King ( 1983 , Pl. Vf).
A well-developed embryophore of large dark cells was
also found in Urceolipora nana (Fig. 1.23B ). As in R. regalis , the polypide in this species degenerates during incubation. In contrast, it remains functional in Mollia multijuncta ,
in which embryos are nourished in immersed ovicells. The
epithelial cells of the embryophore, mainly oval in the upper
and middle parts of the embryophore and cylindrical in the
lower part, stain deeply (Fig. 1.28C ). The activity of the placental analogue declines towards the end of embryogenesis,
and, in ovicells containing a larva, embryophore epithelial
cells are fl at (Fig. 1.28D ) (Ostrovsky 2013 ).
Embryophores develop in all catenicellids studied, of
which only Pterocella scutella was classifi ed as having
reproductive pattern III. In this species, the embryophore
consists of intensely staining columnar and oval epithelial
cells associated with paler funicular cells that, in turn, are
connected with a three-dimensional funicular network in the
zooid cavity (Fig. 1.24A ). The cytoplasm of the epithelial
cells is fi nely granular, sometimes with pale vacuoles, and
nuclei are positioned in the basal part of the cell. Large oval
cells (presumed to be “nutrient storage cells”) are often
found between the funicular cords and on the zooid wall.
It should be noted again that, in Pterocella scutella , both
of the urceoliporids and often also Bugula fl abellatа (see
Dyrynda and Ryland 1982 ), matrotrophic brooding is accompanied by degeneration of the polypide in the maternal zooid.
The virtual absence of the polypide in catenicellids (there
represented by scattered groups of cells remaining of the
brown body) seems to indicate that it is used as one of the
sources of extraembryonic nutrition (see Ryland 1976 ).
1.2.5.3 Bacterial Symbionts
It was discovered that, while the embryo continues to occupy
the ovicell in Bugula fl abellatа , the ooecial vesicle and
adjoining area of the maternal cystid have many large oval or
rounded “bodies” (swollen areas of the funicular cords) that
contain large pale vacuoles and numerous bacteria
(Fig. 1.18B ). They were especially numerous in the cavity of
the ooecial vesicle. If the ovicell was empty, these bodies, if
any, were much less numerous (Fig. 1.18A ).
Bacteria-containing vestibular glands and “funicular bodies”
were fi rst described in cheilostomes, including bugulids, by
Lutaud ( 1964 , 1965 , 1969 ; see also Lutaud 1986 ). Woollacott
and Zimmer ( 1975 ) reported bacterial symbionts inside the
canals of funicular cords approaching the embryophore in
B . neritina and inside the larvae of three Bugula species and
one Watersipora species (see Woollacott 1981 ; Zimmer and
Woollacott 1983 ). A recent study demonstrated that these
bacteria produce substances that act as repellents protecting
the larvae from predation by juvenile fi sh (Lopanik et al.
2004 ). How the bacteria infect the larvae remains unknown.
Zimmer and Woollacott ( 1983 ) suggested that this happens
right after larval release in W . cucullata while the larva is
tethered to the colony by a strand of mucus.
1.2.6 Reproductive Pattern IV
in Cheilostomata
This pattern of sexual reproduction has been described only
recently (Ostrovsky 2009 , 2013 ; Ostrovsky et al. 2009a ;
Moosbrugger et al. 2012 ). It is characterized by precocious
intraovarian fertilization and successive maturation in the
ovary of several macrolecithal oocytes, which are transferred
into a specialized brood chamber where they develop into a
non-feeding ciliated larva. Embryonic development is
accompanied by extraembryonic nutrition at the expense of
the hypertrophied epithelium of the wall of the maternal
zooid and funicular strands. The cells of the embryophore
are activated during brooding of the embryo and enlarge
anew each time an embryo is brooded. Thus, reproductive
pattern IV combines features of patterns II and III.
The description of reproductive pattern IV will begin with
the example of Celleporella hyalina (Hippothoidae).
Oogenesis and a placenta-like system were fi rst studied in
this species by Hughes ( 1987 ), and his data will be used,
supplemented by my own fi ndings.
1.2.6.1 Ovary Structure, Oogenesis and Brooding
in Celleporella hyalina
The structure of the ovary in Celleporella hyalina is similar
to species with reproductive pattern III. On the other hand, it
produces macrolecithal (though small) oocytes (Ostrovsky
1998 , 2013 ). An ovary with immature oocytes is usually suspended on funicular cords in the middle or proximal part of
the coelom of the female polymorph (Figs. 1.26B–F , 1.27D
and 1.36A, B ). At this stage, the gonad is characteristically
“non-compact”: oocytes and oogonia often appear spaced
apart in sections (Fig. 1.26B ). Sometimes one of the oocyte
doublets is located near the basal wall of the cystid or makes
contact with it, whereas the other is suspended in its cavity.
After maturation, the leading oocyte occupies most of the
zooid cavity (Fig. 1.27A, B ). The upper part of the ovary
often adjoins the lower wall of the compensation sac of the
maternal zooid (Figs. 1.26E, F and 1.27D ).
The female gonad consists of a relatively small number of
cells surrounding the oocytes. The upper and lateral walls of
1.2 Reproductive Patterns of Bryozoa
potential hypothesis is that these cells function as “nutrient
storage cells”. Such cells, round or oval and ca. 8–15 μm
diameter, were fi rst described in Bugula fl abellatа by
Dyrynda and King ( 1983 , p. 487). They were found to be
abundant throughout the cystid in my material too
(Fig. 1.18E ), often associated with funicular cords where
they were in contact with the zooid wall. They stain deeply
and sometimes contain large pale vacuoles, also illustrated
by Dyrynda and King ( 1983 , Pl. Vf).
A well-developed embryophore of large dark cells was
also found in Urceolipora nana (Fig. 1.23B ). As in R. regalis , the polypide in this species degenerates during incubation. In contrast, it remains functional in Mollia multijuncta ,
in which embryos are nourished in immersed ovicells. The
epithelial cells of the embryophore, mainly oval in the upper
and middle parts of the embryophore and cylindrical in the
lower part, stain deeply (Fig. 1.28C ). The activity of the placental analogue declines towards the end of embryogenesis,
and, in ovicells containing a larva, embryophore epithelial
cells are fl at (Fig. 1.28D ) (Ostrovsky 2013 ).
Embryophores develop in all catenicellids studied, of
which only Pterocella scutella was classifi ed as having
reproductive pattern III. In this species, the embryophore
consists of intensely staining columnar and oval epithelial
cells associated with paler funicular cells that, in turn, are
connected with a three-dimensional funicular network in the
zooid cavity (Fig. 1.24A ). The cytoplasm of the epithelial
cells is fi nely granular, sometimes with pale vacuoles, and
nuclei are positioned in the basal part of the cell. Large oval
cells (presumed to be “nutrient storage cells”) are often
found between the funicular cords and on the zooid wall.
It should be noted again that, in Pterocella scutella , both
of the urceoliporids and often also Bugula fl abellatа (see
Dyrynda and Ryland 1982 ), matrotrophic brooding is accompanied by degeneration of the polypide in the maternal zooid.
The virtual absence of the polypide in catenicellids (there
represented by scattered groups of cells remaining of the
brown body) seems to indicate that it is used as one of the
sources of extraembryonic nutrition (see Ryland 1976 ).
1.2.5.3 Bacterial Symbionts
It was discovered that, while the embryo continues to occupy
the ovicell in Bugula fl abellatа , the ooecial vesicle and
adjoining area of the maternal cystid have many large oval or
rounded “bodies” (swollen areas of the funicular cords) that
contain large pale vacuoles and numerous bacteria
(Fig. 1.18B ). They were especially numerous in the cavity of
the ooecial vesicle. If the ovicell was empty, these bodies, if
any, were much less numerous (Fig. 1.18A ).
Bacteria-containing vestibular glands and “funicular bodies”
were fi rst described in cheilostomes, including bugulids, by
Lutaud ( 1964 , 1965 , 1969 ; see also Lutaud 1986 ). Woollacott
and Zimmer ( 1975 ) reported bacterial symbionts inside the
canals of funicular cords approaching the embryophore in
B . neritina and inside the larvae of three Bugula species and
one Watersipora species (see Woollacott 1981 ; Zimmer and
Woollacott 1983 ). A recent study demonstrated that these
bacteria produce substances that act as repellents protecting
the larvae from predation by juvenile fi sh (Lopanik et al.
2004 ). How the bacteria infect the larvae remains unknown.
Zimmer and Woollacott ( 1983 ) suggested that this happens
right after larval release in W . cucullata while the larva is
tethered to the colony by a strand of mucus.
1.2.6 Reproductive Pattern IV
in Cheilostomata
This pattern of sexual reproduction has been described only
recently (Ostrovsky 2009 , 2013 ; Ostrovsky et al. 2009a ;
Moosbrugger et al. 2012 ). It is characterized by precocious
intraovarian fertilization and successive maturation in the
ovary of several macrolecithal oocytes, which are transferred
into a specialized brood chamber where they develop into a
non-feeding ciliated larva. Embryonic development is
accompanied by extraembryonic nutrition at the expense of
the hypertrophied epithelium of the wall of the maternal
zooid and funicular strands. The cells of the embryophore
are activated during brooding of the embryo and enlarge
anew each time an embryo is brooded. Thus, reproductive
pattern IV combines features of patterns II and III.
The description of reproductive pattern IV will begin with
the example of Celleporella hyalina (Hippothoidae).
Oogenesis and a placenta-like system were fi rst studied in
this species by Hughes ( 1987 ), and his data will be used,
supplemented by my own fi ndings.
1.2.6.1 Ovary Structure, Oogenesis and Brooding
in Celleporella hyalina
The structure of the ovary in Celleporella hyalina is similar
to species with reproductive pattern III. On the other hand, it
produces macrolecithal (though small) oocytes (Ostrovsky
1998 , 2013 ). An ovary with immature oocytes is usually suspended on funicular cords in the middle or proximal part of
the coelom of the female polymorph (Figs. 1.26B–F , 1.27D
and 1.36A, B ). At this stage, the gonad is characteristically
“non-compact”: oocytes and oogonia often appear spaced
apart in sections (Fig. 1.26B ). Sometimes one of the oocyte
doublets is located near the basal wall of the cystid or makes
contact with it, whereas the other is suspended in its cavity.
After maturation, the leading oocyte occupies most of the
zooid cavity (Fig. 1.27A, B ). The upper part of the ovary
often adjoins the lower wall of the compensation sac of the
maternal zooid (Figs. 1.26E, F and 1.27D ).
The female gonad consists of a relatively small number of
cells surrounding the oocytes. The upper and lateral walls of
1.2 Reproductive Patterns of Bryozoa