51
1.3.3 Structure of the Ovary in Brooding
Cheilostomes
Many early authors illustrated and described the ovary wall
as a fi ne, unstructured membrane (Nitsche 1869 ; Joliet
1877 ; etc.; see also Appendix I for historical details). Smitt
( 1865 ) was one of the fi rst to depict it as consisting of cells,
at least in part, and Claparède ( 1871 ) showed the cells as
fl at. Salensky ( 1874 ) wrote that the ovary consisted of two
layers, an internal one composed of rounded cells [apparently meaning oocytes] and an external one composed of
fl at, spindle- shaped cells [follicle cells]. Repiahoff ( 1876 , р.
140) described the ovary in greater detail – the “eggs” were
surrounded by a thin “cellular membrane,” i.e. a thin unicellular layer [of the follicle], which, together with a group of
cells forming the basis of the ovary, comprised the ovary
wall. Calvet ( 1900 , p. 293) also referred to the follicle wall
as a “cellular membrane”.
Vigelius ( 1884b , 1886 ) gave the most accurate description of the cheilostome ovary for his time, in Chartella membranaceotruncata and Bugula calathus . He described in the
former species how the cells of the ovary wall (which he
called a follicle) were tightly packed, intensely staining,
large, and pear-shaped or cylindrical on the side adjoining
the cystid wall, but pale and fl attened on the opposite side.
The contact zone between the ovary and the cystid could be
vast or tiny, the ovary becoming “pedunculate” in the latter
instance. In comparing ovary structure in the two species, he
noted a signifi cant difference between them. In contrast to
the situation described above, the ovary wall in B . calathus
was represented only by a few small, loosely arranged, fl attened cells. In a couple of instances he also depicted several
small bodies situated between the ovary wall and the oocytes.
It seems that Vigelius actually saw basal cells ( 1884b ), later
depicted also without comment by Calvet ( 1900 , pl. 3,
fi g. 14, inter alia ).
Differences in ovarian structure were also noted by
Waters ( 1912 , рp. 496–497, 1913 ), who actually suggested
assigning bryozoans to two groups depending on the number
and size of oocytes in the ovary – those with “bicellular”
and those with “multicellular” ovaries. He included Bugula
and Bicellariella , with two to three small oocytes, to the fi rst
group, and Scrupocellaria , Canda , Caberea , Bugulopsis
and Menipea , characterized by “many ovarian cells, one or
more of which often attain to a considerable size,” to the
second group.
As noted above, the terms “basal cells” and “subovarian
space” were introduced by Hageman ( 1983 ; see also Reed
1991). However, the fi rst researcher to describe and depict
this part of the female gonad (in Thalamoporella evelinae )
was Marcus ( 1941a ); he noted a narrow basal part (“peduncle”)
that consisted of pale, somewhat elongated cells, which
surround the canal – a slit-like cavity between the cells in the
lower part of the ovary. Reed ( 1991 ) remarked that this
cavity was similar to the “subovarian space” discovered by
Hageman in Membranipora serrilamella . Notwithstanding,
this part of the ovary was subsequently overlooked even by
those who studied ovarian ultrastructure.
Dyrynda and King ( 1983 ) described and illustrated the
structure of the follicular epithelium in Chartella papyracea ,
stating that it differentiates into inner squamous and outer
columnar layers during vitellogenesis. It is rather probable
that columnar cells constitute the ovary wall, whereas the
squamous layer is supposedly formed by fl at basal cells
enveloping the growing oocyte beneath the columnar one,
but available information is too inadequate to be certain.
Intercellular spaces in the lower part of the ovary were subsequently described in Cribrilina annulata (Ostrovsky 1998 )
(see also Fig. 1.10D ).
My own results and data from the literature show that
ovarian structure and function are generally similar in all of
the brooding cheilostomes that have been studied. Observed
differences are likely to be explained by the “productivity”
characters of the ovary, i.e. by the number and properties of
the oocytes formed in it. Small ovary size and few constituent
cells appear to be correlated with the formation of only a
few relatively small oocytes, which is mostly characteristic
of matrotrophic species with reproductive pattern III. By
way of comparison, in most brooding bryozoans lacking
placental analogues, larger oocytes are formed in the ovary,
while in non-brooding malacostegans the ovary contains
many oocytes; in both instances, therefore, ovary cells are
larger and/or more numerous. A comparison of ovaries in
Beania bilaminata and Celleporella hyalina (both with pattern IV) and Gregarinidra serrata and two Bugula species
(pattern III) demonstrates the possibility of transition from
pattern II- and IV-type ovaries to pattern III by means of
progressive reduction of both the total number of ovary cells
and of the intraovarian zone. The ovary in B . bilaminata
(pattern IV) (Fig. 1.21 , inset) retains the main features of
pattern II (Fig. 1.5A, B ), but in C . hyalina (pattern IV)
(Figs. 1.26 and 1.27 ) and Bugula (pattern III) (Fig. 1.18C,
F ) basal cells could not be identifi ed by light microscopy
and the intraovarian zone was represented only by very
small, narrow spaces between the ovary wall and the
oocytes. Gregarinidra serrata (pattern III) (Fig. 1.17 , inset)
demonstrates an intermediate condition. Moreover, when
the ovary of this species contained a mature oocyte, it more
closely resembled that in Callopora (recognizable intraovarian space and basal cells), but when there was no large
oocyte, it resembled that in Bugula . These observations support the idea about the correspondence between ovary structure and the number and type of the gametes produced.
This correspondence, however, is at variance with the situation in Steginoporella perplexa (pattern II) (Fig. 1.12B, D ),
which has very large macrolecithal oocytes and a Bugula - like
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
1.3.3 Structure of the Ovary in Brooding
Cheilostomes
Many early authors illustrated and described the ovary wall
as a fi ne, unstructured membrane (Nitsche 1869 ; Joliet
1877 ; etc.; see also Appendix I for historical details). Smitt
( 1865 ) was one of the fi rst to depict it as consisting of cells,
at least in part, and Claparède ( 1871 ) showed the cells as
fl at. Salensky ( 1874 ) wrote that the ovary consisted of two
layers, an internal one composed of rounded cells [apparently meaning oocytes] and an external one composed of
fl at, spindle- shaped cells [follicle cells]. Repiahoff ( 1876 , р.
140) described the ovary in greater detail – the “eggs” were
surrounded by a thin “cellular membrane,” i.e. a thin unicellular layer [of the follicle], which, together with a group of
cells forming the basis of the ovary, comprised the ovary
wall. Calvet ( 1900 , p. 293) also referred to the follicle wall
as a “cellular membrane”.
Vigelius ( 1884b , 1886 ) gave the most accurate description of the cheilostome ovary for his time, in Chartella membranaceotruncata and Bugula calathus . He described in the
former species how the cells of the ovary wall (which he
called a follicle) were tightly packed, intensely staining,
large, and pear-shaped or cylindrical on the side adjoining
the cystid wall, but pale and fl attened on the opposite side.
The contact zone between the ovary and the cystid could be
vast or tiny, the ovary becoming “pedunculate” in the latter
instance. In comparing ovary structure in the two species, he
noted a signifi cant difference between them. In contrast to
the situation described above, the ovary wall in B . calathus
was represented only by a few small, loosely arranged, fl attened cells. In a couple of instances he also depicted several
small bodies situated between the ovary wall and the oocytes.
It seems that Vigelius actually saw basal cells ( 1884b ), later
depicted also without comment by Calvet ( 1900 , pl. 3,
fi g. 14, inter alia ).
Differences in ovarian structure were also noted by
Waters ( 1912 , рp. 496–497, 1913 ), who actually suggested
assigning bryozoans to two groups depending on the number
and size of oocytes in the ovary – those with “bicellular”
and those with “multicellular” ovaries. He included Bugula
and Bicellariella , with two to three small oocytes, to the fi rst
group, and Scrupocellaria , Canda , Caberea , Bugulopsis
and Menipea , characterized by “many ovarian cells, one or
more of which often attain to a considerable size,” to the
second group.
As noted above, the terms “basal cells” and “subovarian
space” were introduced by Hageman ( 1983 ; see also Reed
1991). However, the fi rst researcher to describe and depict
this part of the female gonad (in Thalamoporella evelinae )
was Marcus ( 1941a ); he noted a narrow basal part (“peduncle”)
that consisted of pale, somewhat elongated cells, which
surround the canal – a slit-like cavity between the cells in the
lower part of the ovary. Reed ( 1991 ) remarked that this
cavity was similar to the “subovarian space” discovered by
Hageman in Membranipora serrilamella . Notwithstanding,
this part of the ovary was subsequently overlooked even by
those who studied ovarian ultrastructure.
Dyrynda and King ( 1983 ) described and illustrated the
structure of the follicular epithelium in Chartella papyracea ,
stating that it differentiates into inner squamous and outer
columnar layers during vitellogenesis. It is rather probable
that columnar cells constitute the ovary wall, whereas the
squamous layer is supposedly formed by fl at basal cells
enveloping the growing oocyte beneath the columnar one,
but available information is too inadequate to be certain.
Intercellular spaces in the lower part of the ovary were subsequently described in Cribrilina annulata (Ostrovsky 1998 )
(see also Fig. 1.10D ).
My own results and data from the literature show that
ovarian structure and function are generally similar in all of
the brooding cheilostomes that have been studied. Observed
differences are likely to be explained by the “productivity”
characters of the ovary, i.e. by the number and properties of
the oocytes formed in it. Small ovary size and few constituent
cells appear to be correlated with the formation of only a
few relatively small oocytes, which is mostly characteristic
of matrotrophic species with reproductive pattern III. By
way of comparison, in most brooding bryozoans lacking
placental analogues, larger oocytes are formed in the ovary,
while in non-brooding malacostegans the ovary contains
many oocytes; in both instances, therefore, ovary cells are
larger and/or more numerous. A comparison of ovaries in
Beania bilaminata and Celleporella hyalina (both with pattern IV) and Gregarinidra serrata and two Bugula species
(pattern III) demonstrates the possibility of transition from
pattern II- and IV-type ovaries to pattern III by means of
progressive reduction of both the total number of ovary cells
and of the intraovarian zone. The ovary in B . bilaminata
(pattern IV) (Fig. 1.21 , inset) retains the main features of
pattern II (Fig. 1.5A, B ), but in C . hyalina (pattern IV)
(Figs. 1.26 and 1.27 ) and Bugula (pattern III) (Fig. 1.18C,
F ) basal cells could not be identifi ed by light microscopy
and the intraovarian zone was represented only by very
small, narrow spaces between the ovary wall and the
oocytes. Gregarinidra serrata (pattern III) (Fig. 1.17 , inset)
demonstrates an intermediate condition. Moreover, when
the ovary of this species contained a mature oocyte, it more
closely resembled that in Callopora (recognizable intraovarian space and basal cells), but when there was no large
oocyte, it resembled that in Bugula . These observations support the idea about the correspondence between ovary structure and the number and type of the gametes produced.
This correspondence, however, is at variance with the situation in Steginoporella perplexa (pattern II) (Fig. 1.12B, D ),
which has very large macrolecithal oocytes and a Bugula - like
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata