47
embryophore cells do not necessarily indicate reduced
effectiveness. In Cellaria fi stulosa (pattern III), a larva
formed from a small microlecithal oocyte fi lls the entire
brood cavity by the end of incubation, whereas the cells of
the embryophore increase little in the course of brooding
(Fig. 1.19B–D ). Different aspects of placental evolution in
Bryozoa are further discussed in Sect. 3.3 .
1.2.7 Reproductive Pattern V
in Cheilostomata
The distinctive mode of sexual reproduction in epistomiid
cheilostomes comprises pattern V (see Ostrovsky et al.
2009a ; Ostrovsky 2009 , 2013 ). In contrast to all other cheilostomes, epistomiids are viviparous, being characterized by
intraovarian incubation with extraembryonic nutrition
assisted by “follicle cells” surrounding the oocyte and
embryo (Marcus 1941b ; Dyrynda 1981 ; Dyrynda and King
1982 , p. 345). This variant is reminiscent of reproduction in
bryozoans of the order Cyclostomata. One ( Epistomia bursaria ) or 2–3 ( Synnotum sp.) small oocytes (alecithal in
Epistomia ) are formed in the maternal zooid but only a single
larva is produced per female zooid. Since the polypide
degenerates, extraembryonic nutrition is ensured by the
transport of substances from other zooids via the funicular
network. Embryo enlargement ranges from 50 to 60-fold
( Synnotum ) to 1,000-fold ( Epistomia ). The origin of the
above-mentioned “follicle” cells, also referred to as “nurse”
cells, is unknown. Dyrynda and King ( 1982 , p. 345) suggested that they are formed from germ cells in “cytoplasmic
continuity” with the oocyte. Complete cytoplasmic bridges
between them were not observed in sections, however, and
this question requires further investigation.
1.2.8 Fertilization
The length of the sperm head in the brooding species studied
varies from 4 to 4.5 μm ( Corbulipora tubulifera ) to 14 μm
( Isoschizoporella secunda ). Within a genus this parameter is
constant ( Tegella 8 μm, Bugula 6 μm, Dendrobeania 8 μm,
Cellaria 6 μm, Calwellia 7 μm, Rhynchozoon 6 μm), almost
constant ( Porella 10–11 μm, Schizomavella 5–6 μm,
Hippoporina 5–5.5 μm, Calyptotheca 5.5–6 μm), or varies
( Arachnopusia unicornis 8 μm vs Arachnopusia sp. 12 μm;
5.5–10 μm in different Smittina species).
The same situation is observed in different families. In
some (Candidae, Bitectiporidae) the length of the sperm
head varies only slightly, whereas in others (Cribrilinidae,
Smittinidae) the range is considerable. In most fl ustrids the
length of the sperm head is 10–11 μm, but in Gregarinidra
serrata it is only half as much (5.5–6 μm) (see Table 1.3 ).
Movement of sperm towards a recipient colony is facilitated
by lophophore-generated water currents (Silén 1966 , 1972 ;
Temkin 1994 ). Sperm enter the cavity of the egg-producing
zooid (insemination) presumably via the supraneural coelomopore (Ostrovsky and Porter 2011 ).
Once in the cavity of the maternal autozooid, sperm
move towards the ovary and penetrate it, prior to fertilization
(Fig. 1.35A, B ). Fourteen sperm were found in a single
ovary of Tegella armifera , not counting those in previtellogenic or vitellogenic oocytes (Fig. 1.35B–D ). Sperm
were also noted in the ovaries of many other species. For
instance, up to 15 sperm were noted in the intraovarian
zone in Bugulopsis monotrypa and Pacifi cincola insculpta
(Ostrovsky 2008b ).
Some of the male gametes that enter the ovary fuse with
oocytes, while the others remain between ovarian cells,
apparently fertilizing later oocytes as they are produced.
These fi ndings support the data of Marcus ( 1938a ) and
Temkin ( 1996 ), who proved that fertilization in brooding
cheilostomes occurs prior to ovulation (but see Silén 1945 ).
Judging from the location of sperm in the intraovarian zone
[directly below the vitellogenic oocyte, between the latter
and the previtellogenic doublet(s) or, more rarely, between
the cells of the previtellogenic doublet and the columnar
epithelium of the ovary wall (Fig. 1.35A, B )], they penetrate ovary in places where the wall has the loosest structure, that is, on the side of the intraovarian zone. In
Hiantopora ferox , two sperm were found between the cells
of lateral ovary wall.
The youngest previtellogenic oocytes with a male pronucleus in Tegella unicornis were only 10 μm diameter, the
length of sperm head being 8 μm. A large, comma-shaped
male pronucleus nested inside the oocyte (Fig. 1.35C ). Thus,
syngamy probably occurs at the end of oogonial mitosis. In
histological sections, early fertilized doublets sometimes
contained differentially stained siblings; the fertilized oocyte
has paler cytoplasm (Fig. 1.13 , inset). The fusion of pronuclei is considerably delayed, since meiosis of the mature
oocyte occurs only after it is transferred to a brood chamber
(see above).
In Celleporella hyalina two to three (up to six) sperm
were found between the cells of the ovary in its lower part
(Fig. 1.26D ). Male pronuclei were also found in previtellogenic oocytes.
In many species, embryos in brood chambers were seen to
be surrounded by a fertilization envelope (Figs. 1.17B ,
1.18B, G , 1.25A and 1.33B ). In rare instances ( Tegella ), it
could not be seen, probably because its wall was too
thin and/or because it was tightly pressed against the embryo.
The fertilization envelope may remain in the ovicell following larval release ( Callopora lineata , C . dumerilii ), its
presence in the brood chamber being an indication of
whether the ovicell was used at least once. In contrast,
1.2 Reproductive Patterns of Bryozoa
embryophore cells do not necessarily indicate reduced
effectiveness. In Cellaria fi stulosa (pattern III), a larva
formed from a small microlecithal oocyte fi lls the entire
brood cavity by the end of incubation, whereas the cells of
the embryophore increase little in the course of brooding
(Fig. 1.19B–D ). Different aspects of placental evolution in
Bryozoa are further discussed in Sect. 3.3 .
1.2.7 Reproductive Pattern V
in Cheilostomata
The distinctive mode of sexual reproduction in epistomiid
cheilostomes comprises pattern V (see Ostrovsky et al.
2009a ; Ostrovsky 2009 , 2013 ). In contrast to all other cheilostomes, epistomiids are viviparous, being characterized by
intraovarian incubation with extraembryonic nutrition
assisted by “follicle cells” surrounding the oocyte and
embryo (Marcus 1941b ; Dyrynda 1981 ; Dyrynda and King
1982 , p. 345). This variant is reminiscent of reproduction in
bryozoans of the order Cyclostomata. One ( Epistomia bursaria ) or 2–3 ( Synnotum sp.) small oocytes (alecithal in
Epistomia ) are formed in the maternal zooid but only a single
larva is produced per female zooid. Since the polypide
degenerates, extraembryonic nutrition is ensured by the
transport of substances from other zooids via the funicular
network. Embryo enlargement ranges from 50 to 60-fold
( Synnotum ) to 1,000-fold ( Epistomia ). The origin of the
above-mentioned “follicle” cells, also referred to as “nurse”
cells, is unknown. Dyrynda and King ( 1982 , p. 345) suggested that they are formed from germ cells in “cytoplasmic
continuity” with the oocyte. Complete cytoplasmic bridges
between them were not observed in sections, however, and
this question requires further investigation.
1.2.8 Fertilization
The length of the sperm head in the brooding species studied
varies from 4 to 4.5 μm ( Corbulipora tubulifera ) to 14 μm
( Isoschizoporella secunda ). Within a genus this parameter is
constant ( Tegella 8 μm, Bugula 6 μm, Dendrobeania 8 μm,
Cellaria 6 μm, Calwellia 7 μm, Rhynchozoon 6 μm), almost
constant ( Porella 10–11 μm, Schizomavella 5–6 μm,
Hippoporina 5–5.5 μm, Calyptotheca 5.5–6 μm), or varies
( Arachnopusia unicornis 8 μm vs Arachnopusia sp. 12 μm;
5.5–10 μm in different Smittina species).
The same situation is observed in different families. In
some (Candidae, Bitectiporidae) the length of the sperm
head varies only slightly, whereas in others (Cribrilinidae,
Smittinidae) the range is considerable. In most fl ustrids the
length of the sperm head is 10–11 μm, but in Gregarinidra
serrata it is only half as much (5.5–6 μm) (see Table 1.3 ).
Movement of sperm towards a recipient colony is facilitated
by lophophore-generated water currents (Silén 1966 , 1972 ;
Temkin 1994 ). Sperm enter the cavity of the egg-producing
zooid (insemination) presumably via the supraneural coelomopore (Ostrovsky and Porter 2011 ).
Once in the cavity of the maternal autozooid, sperm
move towards the ovary and penetrate it, prior to fertilization
(Fig. 1.35A, B ). Fourteen sperm were found in a single
ovary of Tegella armifera , not counting those in previtellogenic or vitellogenic oocytes (Fig. 1.35B–D ). Sperm
were also noted in the ovaries of many other species. For
instance, up to 15 sperm were noted in the intraovarian
zone in Bugulopsis monotrypa and Pacifi cincola insculpta
(Ostrovsky 2008b ).
Some of the male gametes that enter the ovary fuse with
oocytes, while the others remain between ovarian cells,
apparently fertilizing later oocytes as they are produced.
These fi ndings support the data of Marcus ( 1938a ) and
Temkin ( 1996 ), who proved that fertilization in brooding
cheilostomes occurs prior to ovulation (but see Silén 1945 ).
Judging from the location of sperm in the intraovarian zone
[directly below the vitellogenic oocyte, between the latter
and the previtellogenic doublet(s) or, more rarely, between
the cells of the previtellogenic doublet and the columnar
epithelium of the ovary wall (Fig. 1.35A, B )], they penetrate ovary in places where the wall has the loosest structure, that is, on the side of the intraovarian zone. In
Hiantopora ferox , two sperm were found between the cells
of lateral ovary wall.
The youngest previtellogenic oocytes with a male pronucleus in Tegella unicornis were only 10 μm diameter, the
length of sperm head being 8 μm. A large, comma-shaped
male pronucleus nested inside the oocyte (Fig. 1.35C ). Thus,
syngamy probably occurs at the end of oogonial mitosis. In
histological sections, early fertilized doublets sometimes
contained differentially stained siblings; the fertilized oocyte
has paler cytoplasm (Fig. 1.13 , inset). The fusion of pronuclei is considerably delayed, since meiosis of the mature
oocyte occurs only after it is transferred to a brood chamber
(see above).
In Celleporella hyalina two to three (up to six) sperm
were found between the cells of the ovary in its lower part
(Fig. 1.26D ). Male pronuclei were also found in previtellogenic oocytes.
In many species, embryos in brood chambers were seen to
be surrounded by a fertilization envelope (Figs. 1.17B ,
1.18B, G , 1.25A and 1.33B ). In rare instances ( Tegella ), it
could not be seen, probably because its wall was too
thin and/or because it was tightly pressed against the embryo.
The fertilization envelope may remain in the ovicell following larval release ( Callopora lineata , C . dumerilii ), its
presence in the brood chamber being an indication of
whether the ovicell was used at least once. In contrast,
1.2 Reproductive Patterns of Bryozoa