40
could be even more numerous in nurse cells than in oocytes.
Yolk granules were noted in the nurse cells of species pairs in
three genera: Dendrobeania fruticosa and D . quadridentata ,
Porella smitti and P . minuta , Hippoporina reticulatopunctata and H . propinqua (see Table 1.7 ).
In the latter species the parameters of oogenesis were
highly variable: (1) nurse cells in some mature oocyte doublets were smaller than those of previtellogenic doublets;
(2) the number of vitellogenic doublets in the ovary could
be one or two; (3) in the latter instance the number of yolk
granules in the larger vitellogenic oocyte could be rather
fewer than in the smaller one; (4) oocytes of different size
could initiate vitellogenesis, no limiting infl uence of any
other oocyte doublets (including the leading one) having
being noted; (5) yolk granules could be absent in early and
even mid-stage nurse cells but were always present in
mature ones. Some of these features were also observed in
other species, but in H . propinqua they were especially
prominent.
Enlargement of Oocytes and Embryos
Oocyte volume can increase by a factor of 100, 1,000 and
sometimes 10,000 while in the ovary, the minimum calculated enlargement being 324.9-fold in Crepidacantha kirkpatricki (Crepidacanthidae) and the maximum 98,328.2-fold
in Nematofl ustra fl agellata (Flustridae). During vitellogenesis, oocyte volume increases as a rule by a factor of 10, more
rarely by a factor of 100. The minimum calculated enlargement was in this case eight-fold in Exochella sp., with a
maximum of 681-fold in Eurystomella foraminigera (see
Table 1.6 ).
Following ovulation, the mature primary oocyte is transferred to the brood chamber by active movements of the polypide, and polar bodies separate from it (reviewed in Reed
1991 ; Ostrovsky et al. 2008 ). A secondary oocyte is formed
following separation of the fi rst polar body and an egg following separation of the second. In an egg with a male pronucleus karyogamy takes place, resulting in the formation of
the zygote, which starts to cleave.
Embryo size was noted to increase during brooding in
several species. This was determined by comparing the volume of late embryos with that of early embryos, zygotes and
mature oocytes. In the absence of late embryos the latter
three parameters were compared. Maximum enlargement
was found in Callopora dumerilii (4.4-fold) and the minimum in Reteporella sp. (1.03-fold) (see Table 1.8 ). Insofar as
species with reproductive pattern II have no extraembryonic
nutrition, it may be supposed that this enlargement results
from compaction of material during cleavage or water uptake
(Ostrovsky 1998 , 2013 ).
As is well known, embryos (and thus eggs) are pigmented
in different bryozoan species, ranging from white and pale
yellow through pink and orange to scarlet, red and crimson.
In a few species eggs and embryos are described as being
colourless (see Ryland 1958 ; Eggleston 1970 ).
1.2.4.3 Parasites
In several colonies of Cribrilina annulata (Cribrilinidae) and
Tegella unicornis (Calloporidae), mature ovarian and ovulated
oocytes were found to contain intracellular parasites of
unknown taxonomic position (Ostrovsky 1998 , 2009 ). A single oocyte could contain from one to three such parasitic
cells, which have a characteristic radially striated cytoplasm.
In early stages of development, the cell membrane of the parasite was unrecognizable by light microscopy (Fig. 1.16A–C ),
while in later stages the borders of these cells with their digitate
projections were clearly seen. At this stage the oocyte nucleus
is deformed and the cytoplasm was separated into two zones –
a central zone with numerous yolk granules and a peripheral
zone with considerably fewer yolk granules. Parasite cells were
noted only in the peripheral zone (Fig. 1.16D ). A spore of this
parasite was found once; its capsule was capped and its content
had the above-mentioned radially striated structure (Fig. 1.16
inset).
1.2.5 Reproductive Pattern III
in Cheilostomata
Reproductive pattern III is characterized by successive maturation in the ovary of several small oligo- or mesolecithal
oocytes. Fertilization is intraovarian and precocious.
Karyogamy is delayed until after oviposition. Oocyte
development is assisted by nurse cells. The mature oocyte is
transferred into the brood chamber where it develops into a
non-feeding ciliated larva. Larval development is accompanied by extraembryonic nutrition (EEN) ensured by the
embryophore, which comprises hypertrophied epithelium of
the maternal-zooid wall and associated cells of the funicular
system. This cell complex is considered to be a placental
analogue, ensuring bidirectional transport of nutrients
between the embryo and the maternal zooid, whose cells are
activated and hypertrophied anew during each brooding
episode, decreasing in size when the brood chamber is
emptied.
Reproductive pattern III has been found in Gregarinidra
serrata (Flustridae), Bugula fl abellata , B . neritina
(Bugulidae), Mollia multijuncta (Microporidae), Cellaria
fi stulosa (Cellariidae), Pterocella scutella (Catenicellidae),
Urceolipora nana and Reciprocus regalis (Urceoliporidae)
(Ostrovsky 2013 ). This pattern should also be characteristic
of Adeonella calveti (Adeonidae), based on the descriptions
of Waters ( 1912 , 1913 ) and my own data (Ostrovsky et al.
2009a ; Ostrovsky 2009 ).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
could be even more numerous in nurse cells than in oocytes.
Yolk granules were noted in the nurse cells of species pairs in
three genera: Dendrobeania fruticosa and D . quadridentata ,
Porella smitti and P . minuta , Hippoporina reticulatopunctata and H . propinqua (see Table 1.7 ).
In the latter species the parameters of oogenesis were
highly variable: (1) nurse cells in some mature oocyte doublets were smaller than those of previtellogenic doublets;
(2) the number of vitellogenic doublets in the ovary could
be one or two; (3) in the latter instance the number of yolk
granules in the larger vitellogenic oocyte could be rather
fewer than in the smaller one; (4) oocytes of different size
could initiate vitellogenesis, no limiting infl uence of any
other oocyte doublets (including the leading one) having
being noted; (5) yolk granules could be absent in early and
even mid-stage nurse cells but were always present in
mature ones. Some of these features were also observed in
other species, but in H . propinqua they were especially
prominent.
Enlargement of Oocytes and Embryos
Oocyte volume can increase by a factor of 100, 1,000 and
sometimes 10,000 while in the ovary, the minimum calculated enlargement being 324.9-fold in Crepidacantha kirkpatricki (Crepidacanthidae) and the maximum 98,328.2-fold
in Nematofl ustra fl agellata (Flustridae). During vitellogenesis, oocyte volume increases as a rule by a factor of 10, more
rarely by a factor of 100. The minimum calculated enlargement was in this case eight-fold in Exochella sp., with a
maximum of 681-fold in Eurystomella foraminigera (see
Table 1.6 ).
Following ovulation, the mature primary oocyte is transferred to the brood chamber by active movements of the polypide, and polar bodies separate from it (reviewed in Reed
1991 ; Ostrovsky et al. 2008 ). A secondary oocyte is formed
following separation of the fi rst polar body and an egg following separation of the second. In an egg with a male pronucleus karyogamy takes place, resulting in the formation of
the zygote, which starts to cleave.
Embryo size was noted to increase during brooding in
several species. This was determined by comparing the volume of late embryos with that of early embryos, zygotes and
mature oocytes. In the absence of late embryos the latter
three parameters were compared. Maximum enlargement
was found in Callopora dumerilii (4.4-fold) and the minimum in Reteporella sp. (1.03-fold) (see Table 1.8 ). Insofar as
species with reproductive pattern II have no extraembryonic
nutrition, it may be supposed that this enlargement results
from compaction of material during cleavage or water uptake
(Ostrovsky 1998 , 2013 ).
As is well known, embryos (and thus eggs) are pigmented
in different bryozoan species, ranging from white and pale
yellow through pink and orange to scarlet, red and crimson.
In a few species eggs and embryos are described as being
colourless (see Ryland 1958 ; Eggleston 1970 ).
1.2.4.3 Parasites
In several colonies of Cribrilina annulata (Cribrilinidae) and
Tegella unicornis (Calloporidae), mature ovarian and ovulated
oocytes were found to contain intracellular parasites of
unknown taxonomic position (Ostrovsky 1998 , 2009 ). A single oocyte could contain from one to three such parasitic
cells, which have a characteristic radially striated cytoplasm.
In early stages of development, the cell membrane of the parasite was unrecognizable by light microscopy (Fig. 1.16A–C ),
while in later stages the borders of these cells with their digitate
projections were clearly seen. At this stage the oocyte nucleus
is deformed and the cytoplasm was separated into two zones –
a central zone with numerous yolk granules and a peripheral
zone with considerably fewer yolk granules. Parasite cells were
noted only in the peripheral zone (Fig. 1.16D ). A spore of this
parasite was found once; its capsule was capped and its content
had the above-mentioned radially striated structure (Fig. 1.16
inset).
1.2.5 Reproductive Pattern III
in Cheilostomata
Reproductive pattern III is characterized by successive maturation in the ovary of several small oligo- or mesolecithal
oocytes. Fertilization is intraovarian and precocious.
Karyogamy is delayed until after oviposition. Oocyte
development is assisted by nurse cells. The mature oocyte is
transferred into the brood chamber where it develops into a
non-feeding ciliated larva. Larval development is accompanied by extraembryonic nutrition (EEN) ensured by the
embryophore, which comprises hypertrophied epithelium of
the maternal-zooid wall and associated cells of the funicular
system. This cell complex is considered to be a placental
analogue, ensuring bidirectional transport of nutrients
between the embryo and the maternal zooid, whose cells are
activated and hypertrophied anew during each brooding
episode, decreasing in size when the brood chamber is
emptied.
Reproductive pattern III has been found in Gregarinidra
serrata (Flustridae), Bugula fl abellata , B . neritina
(Bugulidae), Mollia multijuncta (Microporidae), Cellaria
fi stulosa (Cellariidae), Pterocella scutella (Catenicellidae),
Urceolipora nana and Reciprocus regalis (Urceoliporidae)
(Ostrovsky 2013 ). This pattern should also be characteristic
of Adeonella calveti (Adeonidae), based on the descriptions
of Waters ( 1912 , 1913 ) and my own data (Ostrovsky et al.
2009a ; Ostrovsky 2009 ).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis