48
according to the ТЕМ data of Hughes ( 1987 ), the fertilization
envelope disappears in late embryos of Celleporella
hyalina .
At the same time, in some species the fertilization envelope becomes discernible by light microscopy level while the
oocyte, partly or completely ovulated, is still in the zooid
coelom. For instance, it was clearly visible in mature oocytes
of Porella proboscidea (Fig. 1.13A ), Mucropetraliella ellerii
and Petralia undata . It can also be seen in the paper of
Hughes ( 1987 , Pl. VIIa), which shows the surface of a partly
ovulated oocyte of C . hyalina [see also notes on the illustrations of Vigelius ( 1884b ) in Sect. 1.1 ].
1.3
Comparative Analysis of Sexual
Reproduction in Cheilostomata
Oogenesis in Cheilostomata is alimentary (i.e. polygenic),
that is, the oocyte is intimately associated with accessory
cells, which play an important role in its growth and development. Alimentary oogenesis can be further categorized as
either follicular, with follicle cells as accessory cells, or
nutrimentary, with accessory cells broadly termed nurse cells
(Wourms 1987 ; Dondua 2005 ). In the former instance, synthesis and transport of nutrients is ensured by cells of somatic
origin, namely ovarian cells, while in the latter it is ensured
by nurse cells, which are derivatives of the female gametic
line. Oogenesis in non-brooding cheilostomes lacking nurse
cells (reproductive pattern I) may be classifi ed as follicular.
Although the nutritive role of the follicle cells is still unclear,
it has been shown that the synthesis and transport of yolk
precursors are provided by basal ovarian cells of mesothelial
origin (Hageman 1983 ; see also Reed 1991 ). The data presented above show that oogenesis in Cheilostomata with
reproductive patterns II, III and IV combines the features of
these two variants of alimentary nutrition, with the ovarian
cells and nurse cells actively participating in synthesis and
transport of either nutrients or RNA for the oocyte. Oocytes
surrounded by follicle as well as nurse cells are also known
in many arthropods, especially insects (Raven 1961 ), but
ovary cells are presumed to provide hormonal regulation of
oogenesis in this case (Adiyodi and Adiyodi 1983 ).
Alimentary oogenesis in cheilostomes of the family
Epistomiidae cannot defi nitely be attributed to any of these
variants until the origin of ovary cells is clarifi ed.
The structure of cheilostome ovaries has certain features in
common throughout the order that correspond overall to type
II invertebrate ovaries (Korschelt and Heider 1893 ; Raven
1961 ; Wourms 1987 ). Developing from mesothelial cells, the
ovary is a combination of the outer wall, which surrounds the
oogonia and developing oocytes, and a group of accessory
basal cells, which are in contact with the epithelial lining of
the body wall and the cells of the ovary wall. Other important
features are the presence of an intraovarian zone, the lacunae
of which communicate with those of the funicular cords, and
no gonoduct. Reed ( 1991 ) likened the connection of the ovary
with the funicular system in bryozoans to the interactions
between the ovaries and the circulatory system of some sedentary polychaetes. As for the basal cells, their position and
functions resemble those of the so-called “nutritive phagocytes” that are known in echinoderms and especially well
studied in sea urchins (Wourms 1987 , p. 125). Some nemerteans contain “secondary cells” in the ovary, but their functions
and origin are unknown. The lacunar system of the intraovarian zone in cheilostomes is in some respects similar to the
follicular cavity of the gastropod Limnaea stagnalis . It is
formed between the oocyte and the follicle cells (in the upper
part of the follicle) and its fl uid bathes the surface of the
female gamete (de Jong-Brink et al. 1983 ).
In the gastropod Viviparus viviparus , a mature ovarian
oocyte is partially exposed into the cavity of the ovarian
lobe. In a pentastomid (Arthropoda), the surface area of the
ovarian oocyte exposed to the hemocoel is covered with
microvilli. Microvilli are also found on the surface of ovarian
oocytes in some crustaceans, brachiopods and entoprocts
and on the surface of coelomic oocytes in some sipunculids
and polychaetes (Adiyodi and Adiyodi 1983 ). In some gastropods the polarity of the oocyte is determined by the site of
its contact with follicle cells (de Jong-Brink et al. 1983 ). All
these facts indicate that some features of oogenesis in
Cheilostomata are also characteristic of representatives of
other invertebrate groups.
1.3.1 Early Stages of Oogenesis
Early developmental stages of the ovary in Membranipora
serrilamella (Malacostegina) were briefl y described and
illustrated by Hageman ( 1983 , p. 73, Ill. 3), who noted only
that “the somatic peritoneal cells associated with the funicular ramifi cations [that insert into one of the lateral walls]
participate in the proliferation of oocytes and follicle cells”.
The origin of the ovary on the lateral cystid wall was also
recorded by Grant ( 1827 ) and Vigelius ( 1882 , 1884a , b ) in
fl ustrids. Silbermann ( 1906 ) and Römer ( 1906 ) also stated
that the ovary develops within the epidermal layer of the cystid wall in the ctenostome Alcyonidium mytili.
As for other gymnolaemates, early female cells associated with the developing polypide bud in a newly formed
zooid were described by Claparède ( 1871 ), Repiachoff
( 1875 ), Calvet ( 1900 ) and Ostrovsky ( 1998 ). In contrast with
the above-mentioned fl ustrids, it seems that the ovary develops in association with a polypide bud in Chartella papyracea (see Dyrynda and King 1982 ). Detailed studies of the
early stages of gonado- and gametogenesis have been conducted only on ctenostomes (Pace 1906 ; Faulkner 1933 ;
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
according to the ТЕМ data of Hughes ( 1987 ), the fertilization
envelope disappears in late embryos of Celleporella
hyalina .
At the same time, in some species the fertilization envelope becomes discernible by light microscopy level while the
oocyte, partly or completely ovulated, is still in the zooid
coelom. For instance, it was clearly visible in mature oocytes
of Porella proboscidea (Fig. 1.13A ), Mucropetraliella ellerii
and Petralia undata . It can also be seen in the paper of
Hughes ( 1987 , Pl. VIIa), which shows the surface of a partly
ovulated oocyte of C . hyalina [see also notes on the illustrations of Vigelius ( 1884b ) in Sect. 1.1 ].
1.3
Comparative Analysis of Sexual
Reproduction in Cheilostomata
Oogenesis in Cheilostomata is alimentary (i.e. polygenic),
that is, the oocyte is intimately associated with accessory
cells, which play an important role in its growth and development. Alimentary oogenesis can be further categorized as
either follicular, with follicle cells as accessory cells, or
nutrimentary, with accessory cells broadly termed nurse cells
(Wourms 1987 ; Dondua 2005 ). In the former instance, synthesis and transport of nutrients is ensured by cells of somatic
origin, namely ovarian cells, while in the latter it is ensured
by nurse cells, which are derivatives of the female gametic
line. Oogenesis in non-brooding cheilostomes lacking nurse
cells (reproductive pattern I) may be classifi ed as follicular.
Although the nutritive role of the follicle cells is still unclear,
it has been shown that the synthesis and transport of yolk
precursors are provided by basal ovarian cells of mesothelial
origin (Hageman 1983 ; see also Reed 1991 ). The data presented above show that oogenesis in Cheilostomata with
reproductive patterns II, III and IV combines the features of
these two variants of alimentary nutrition, with the ovarian
cells and nurse cells actively participating in synthesis and
transport of either nutrients or RNA for the oocyte. Oocytes
surrounded by follicle as well as nurse cells are also known
in many arthropods, especially insects (Raven 1961 ), but
ovary cells are presumed to provide hormonal regulation of
oogenesis in this case (Adiyodi and Adiyodi 1983 ).
Alimentary oogenesis in cheilostomes of the family
Epistomiidae cannot defi nitely be attributed to any of these
variants until the origin of ovary cells is clarifi ed.
The structure of cheilostome ovaries has certain features in
common throughout the order that correspond overall to type
II invertebrate ovaries (Korschelt and Heider 1893 ; Raven
1961 ; Wourms 1987 ). Developing from mesothelial cells, the
ovary is a combination of the outer wall, which surrounds the
oogonia and developing oocytes, and a group of accessory
basal cells, which are in contact with the epithelial lining of
the body wall and the cells of the ovary wall. Other important
features are the presence of an intraovarian zone, the lacunae
of which communicate with those of the funicular cords, and
no gonoduct. Reed ( 1991 ) likened the connection of the ovary
with the funicular system in bryozoans to the interactions
between the ovaries and the circulatory system of some sedentary polychaetes. As for the basal cells, their position and
functions resemble those of the so-called “nutritive phagocytes” that are known in echinoderms and especially well
studied in sea urchins (Wourms 1987 , p. 125). Some nemerteans contain “secondary cells” in the ovary, but their functions
and origin are unknown. The lacunar system of the intraovarian zone in cheilostomes is in some respects similar to the
follicular cavity of the gastropod Limnaea stagnalis . It is
formed between the oocyte and the follicle cells (in the upper
part of the follicle) and its fl uid bathes the surface of the
female gamete (de Jong-Brink et al. 1983 ).
In the gastropod Viviparus viviparus , a mature ovarian
oocyte is partially exposed into the cavity of the ovarian
lobe. In a pentastomid (Arthropoda), the surface area of the
ovarian oocyte exposed to the hemocoel is covered with
microvilli. Microvilli are also found on the surface of ovarian
oocytes in some crustaceans, brachiopods and entoprocts
and on the surface of coelomic oocytes in some sipunculids
and polychaetes (Adiyodi and Adiyodi 1983 ). In some gastropods the polarity of the oocyte is determined by the site of
its contact with follicle cells (de Jong-Brink et al. 1983 ). All
these facts indicate that some features of oogenesis in
Cheilostomata are also characteristic of representatives of
other invertebrate groups.
1.3.1 Early Stages of Oogenesis
Early developmental stages of the ovary in Membranipora
serrilamella (Malacostegina) were briefl y described and
illustrated by Hageman ( 1983 , p. 73, Ill. 3), who noted only
that “the somatic peritoneal cells associated with the funicular ramifi cations [that insert into one of the lateral walls]
participate in the proliferation of oocytes and follicle cells”.
The origin of the ovary on the lateral cystid wall was also
recorded by Grant ( 1827 ) and Vigelius ( 1882 , 1884a , b ) in
fl ustrids. Silbermann ( 1906 ) and Römer ( 1906 ) also stated
that the ovary develops within the epidermal layer of the cystid wall in the ctenostome Alcyonidium mytili.
As for other gymnolaemates, early female cells associated with the developing polypide bud in a newly formed
zooid were described by Claparède ( 1871 ), Repiachoff
( 1875 ), Calvet ( 1900 ) and Ostrovsky ( 1998 ). In contrast with
the above-mentioned fl ustrids, it seems that the ovary develops in association with a polypide bud in Chartella papyracea (see Dyrynda and King 1982 ). Detailed studies of the
early stages of gonado- and gametogenesis have been conducted only on ctenostomes (Pace 1906 ; Faulkner 1933 ;
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis