49
Chrétien 1958 ; Owrid and Ryland 1991 ). In all species
studied, precursors of the earliest female cells were also
found in polypide buds, at the stage of a two-layered sac. My
data on Cauloramphus spinifer (Calloporidae) show that, at
least in this species, the site and the time of origin of the
ovary are as in ctenostomes.
Faulkner ( 1933 ) called the precursors of female cells in
the bud of the developing polypide “neoblasts” (in
Alcyonidium gelatinosum ), while Owrid and Ryland ( 1991 )
called them “primordial cells” (in A . hirsutum ). In both
cases, primordial germ cells (PGC) were presumably meant.
Calvet ( 1900 ) and Chrétien ( 1958 ) denoted the next stage as
“cellules ovariennes initiales” and “cellules femelles initiales” (in A . diaphanum ), which were later redefi ned as primary oogonia (reviewed in Hayward 1983 ; see also Owrid
and Ryland 1991 ).
A pair of female gamete cells in the polypide bud in
Cauloramphus spinifer were, judging from their appearance
and time of origin, represented by primary oogonia
(Fig. 1.8A, B ). PGC appear to be impossible to distinguish
from the mesothelial cells of the polypide by light microscopy, whereas oogonia are slightly larger than the latter.
Pairs of still larger female cells found in young ovaries of the
developing polypides in this and several other species
( Scrupocellaria scabra , Cribrilina annulata , Celleporella
hyalina ) are presumably developing oogonia (Figs. 1.10A,
B , 1.12A and 1.26A ).
It appears that, in mature cheilostome ovaries, there is a
small self-replicating group of primary oogonia, whose
divisions result in formation of (1) oocytes (pattern I) and
oocyte doublets (patterns II–IV), and (2) primary oogonia
maintaining the oogonial pool in the ovary. In general, this
is similar to the stereotypical pattern of germ-cell division
and differentiation in other invertebrates, e.g. insects
(Wourms 1987 ; Dondua 2005 ). All of these cells may, in
principle, be the descendants of one or a few PGC, which
appear in the early polypide bud and differentiate into primary oogonia. It may be assumed that in bryozoans, whose
oogenesis proceeds with the formation of oocyte doublets,
each oogonium divides to form an oogonial pair. Instead of
differentiating into a secondary oogonium and then into a
young primary oocyte, as happens in the majority of animals, one of them gives rise to an oocyte doublet and the
second divides to form two oogonia, after which this
sequence is repeated (see Sect. 1.2.4 ). For instance, Calvet
( 1900 ) wrote that early female cells, before becoming “little
eggs”, undergo one division in some species (see also
Chrétien 1958 ). However, inasmuch as Calvet failed to
notice that oocytes are always paired in brooding cheilostomes, it is unclear what he actually described; the division
mentioned may be that of the oogonium resulting in the formation of two daughter oogonia or else that resulting in the
formation of an early oocyte doublet.
The scheme of female-gamete formation suggested above
agrees with the opinion of Vigelius ( 1884b ), who thought
that ovary cells never transform into gametes. On the other
hand, it is theoretically possible that PGC may appear from
time to time in the mature ovary by dedifferentiation of the
somatic cells of its wall, if the initial source of oogonia is
exhausted. As mentioned above, oogonia were not found in
the ovaries of most species studied. Groups of small dividing
cells have been recognized between prismatic cells making
up the wall of mature ovaries in two calloporids ( Callopora
lineata , Tegella unicornis ) (Fig. 1.6B ). We cannot be entirely
sure that these divisions result in formation of PGC or oogonia (they may be associated, for instance, with an increase in
or renewal of the cellular composition of the gonad wall),
and further research is needed to clarify the situation.
1.3.2 Ovary and Oogenesis in Non-brooding
Species
Data on the location of gonads, the number of maturing
oocytes and the ways in which they are released in
Malacostegina are found in more than 20 publications.
The earliest is a paper by Smitt ( 1865 ), who depicted about
40 small ovarian oocytes and fi ve ovulated oocytes in a zooid
of Membranipora membranacea . The position of the ovary
has often been described (Smitt 1865 ; Repiachoff 1876 ;
Joliet 1877 ; Prouho 1892 ; Calvet 1900 ; Schulz 1901 ; Marcus
1926a ; Silén 1945 , 1966 ; Borg 1947 ; Mawatari and Mawatari
1975 ; Hageman 1983 ; Zimmer, cited in Reed 1991 ). It is
located on the basal wall of the cystid (or, more rarely, suspended on funicular cords) in the distal ( M . membranacea ,
M . serrilamella ), middle ( M . membranacea , Electra pilosa )
or proximal part of the fertile zooid ( M . membranacea , M .
serrilamella , Electra repiachowi , E . pilosa , E . posidoniae ,
Einhornia crustulenta ).
Prior to the dissertation of Hageman ( 1983 ), ovary structure and oogenesis in malacostegans had been described in
detail only twice (Calvet 1900 ; Bonnevie 1907 ), with Electra
pilosa the object of study in both cases. Calvet described and
depicted the young and mature ovary, and noted that, in the
latter, follicle cells surrounding the oocytes from above and
the sides become fl attened. He also noted that while some
oocytes enlarge, those underlying them degenerate. Later
degeneration of some oocytes was also recorded by Hageman
( 1983 ) in the ovary of M . serrilamella . As for changes in oocyte
structure, Calvet mostly noted the transformation of their
nuclei. A more detailed study was made by Bonnevie ( 1907 ),
who observed successive stages of oocyte development,
specially recording darker staining of the cytoplasm in young
female gametes and numerous yolk granules in the cytoplasm
of mature ones. According to her data, young oocytes are
located at the periphery of the ovary, where germ cells
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
Chrétien 1958 ; Owrid and Ryland 1991 ). In all species
studied, precursors of the earliest female cells were also
found in polypide buds, at the stage of a two-layered sac. My
data on Cauloramphus spinifer (Calloporidae) show that, at
least in this species, the site and the time of origin of the
ovary are as in ctenostomes.
Faulkner ( 1933 ) called the precursors of female cells in
the bud of the developing polypide “neoblasts” (in
Alcyonidium gelatinosum ), while Owrid and Ryland ( 1991 )
called them “primordial cells” (in A . hirsutum ). In both
cases, primordial germ cells (PGC) were presumably meant.
Calvet ( 1900 ) and Chrétien ( 1958 ) denoted the next stage as
“cellules ovariennes initiales” and “cellules femelles initiales” (in A . diaphanum ), which were later redefi ned as primary oogonia (reviewed in Hayward 1983 ; see also Owrid
and Ryland 1991 ).
A pair of female gamete cells in the polypide bud in
Cauloramphus spinifer were, judging from their appearance
and time of origin, represented by primary oogonia
(Fig. 1.8A, B ). PGC appear to be impossible to distinguish
from the mesothelial cells of the polypide by light microscopy, whereas oogonia are slightly larger than the latter.
Pairs of still larger female cells found in young ovaries of the
developing polypides in this and several other species
( Scrupocellaria scabra , Cribrilina annulata , Celleporella
hyalina ) are presumably developing oogonia (Figs. 1.10A,
B , 1.12A and 1.26A ).
It appears that, in mature cheilostome ovaries, there is a
small self-replicating group of primary oogonia, whose
divisions result in formation of (1) oocytes (pattern I) and
oocyte doublets (patterns II–IV), and (2) primary oogonia
maintaining the oogonial pool in the ovary. In general, this
is similar to the stereotypical pattern of germ-cell division
and differentiation in other invertebrates, e.g. insects
(Wourms 1987 ; Dondua 2005 ). All of these cells may, in
principle, be the descendants of one or a few PGC, which
appear in the early polypide bud and differentiate into primary oogonia. It may be assumed that in bryozoans, whose
oogenesis proceeds with the formation of oocyte doublets,
each oogonium divides to form an oogonial pair. Instead of
differentiating into a secondary oogonium and then into a
young primary oocyte, as happens in the majority of animals, one of them gives rise to an oocyte doublet and the
second divides to form two oogonia, after which this
sequence is repeated (see Sect. 1.2.4 ). For instance, Calvet
( 1900 ) wrote that early female cells, before becoming “little
eggs”, undergo one division in some species (see also
Chrétien 1958 ). However, inasmuch as Calvet failed to
notice that oocytes are always paired in brooding cheilostomes, it is unclear what he actually described; the division
mentioned may be that of the oogonium resulting in the formation of two daughter oogonia or else that resulting in the
formation of an early oocyte doublet.
The scheme of female-gamete formation suggested above
agrees with the opinion of Vigelius ( 1884b ), who thought
that ovary cells never transform into gametes. On the other
hand, it is theoretically possible that PGC may appear from
time to time in the mature ovary by dedifferentiation of the
somatic cells of its wall, if the initial source of oogonia is
exhausted. As mentioned above, oogonia were not found in
the ovaries of most species studied. Groups of small dividing
cells have been recognized between prismatic cells making
up the wall of mature ovaries in two calloporids ( Callopora
lineata , Tegella unicornis ) (Fig. 1.6B ). We cannot be entirely
sure that these divisions result in formation of PGC or oogonia (they may be associated, for instance, with an increase in
or renewal of the cellular composition of the gonad wall),
and further research is needed to clarify the situation.
1.3.2 Ovary and Oogenesis in Non-brooding
Species
Data on the location of gonads, the number of maturing
oocytes and the ways in which they are released in
Malacostegina are found in more than 20 publications.
The earliest is a paper by Smitt ( 1865 ), who depicted about
40 small ovarian oocytes and fi ve ovulated oocytes in a zooid
of Membranipora membranacea . The position of the ovary
has often been described (Smitt 1865 ; Repiachoff 1876 ;
Joliet 1877 ; Prouho 1892 ; Calvet 1900 ; Schulz 1901 ; Marcus
1926a ; Silén 1945 , 1966 ; Borg 1947 ; Mawatari and Mawatari
1975 ; Hageman 1983 ; Zimmer, cited in Reed 1991 ). It is
located on the basal wall of the cystid (or, more rarely, suspended on funicular cords) in the distal ( M . membranacea ,
M . serrilamella ), middle ( M . membranacea , Electra pilosa )
or proximal part of the fertile zooid ( M . membranacea , M .
serrilamella , Electra repiachowi , E . pilosa , E . posidoniae ,
Einhornia crustulenta ).
Prior to the dissertation of Hageman ( 1983 ), ovary structure and oogenesis in malacostegans had been described in
detail only twice (Calvet 1900 ; Bonnevie 1907 ), with Electra
pilosa the object of study in both cases. Calvet described and
depicted the young and mature ovary, and noted that, in the
latter, follicle cells surrounding the oocytes from above and
the sides become fl attened. He also noted that while some
oocytes enlarge, those underlying them degenerate. Later
degeneration of some oocytes was also recorded by Hageman
( 1983 ) in the ovary of M . serrilamella . As for changes in oocyte
structure, Calvet mostly noted the transformation of their
nuclei. A more detailed study was made by Bonnevie ( 1907 ),
who observed successive stages of oocyte development,
specially recording darker staining of the cytoplasm in young
female gametes and numerous yolk granules in the cytoplasm
of mature ones. According to her data, young oocytes are
located at the periphery of the ovary, where germ cells
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata