53
by the nurse cell (absent in Malacostegina), and yolk is
produced by the oocyte itself. The oocytes grow unequally,
with increase in size of the leading oocyte considerably
outstripping the nurse cell.
3. The fi nal (ovulatory) phase begins with partial degradation of the follicle wall. In malacostegans, contact (via
gap junctions) of the follicle cells with oocytes is lost
(Hageman 1983 ). Ovulation is a gradual process, in the
course of which the oocyte may remain in the ovary for
some time, partly exposed to the zooid cavity and sometimes continuing to accumulate reserve nutrients from the
coelomic fl uid by microvilli (Hughes 1987 ). The ovulatory phase is completed upon the release of the oocyte
from the ovary into the coelom, accompanied by degradation of the nurse cell, if any. It is during this phase that
fertilization occurs in malacostegans. The nuclear envelope degrades shortly before ovulation or soon after.
Silén’s ( 1945 ) landmark paper on sexual reproduction in
three bryozoan species with reproductive pattern II was a
major contribution to knowledge of oogenesis in cheilostome
brooders. Overall, the sequence of events is accurately
described in this study, but some observations and conclusions require comment. According to Silén, the ovary of
Callopora dumerilii contains a single oocyte [in fact, a doublet], with a second one appearing only at the fi nal developmental stage of the leading oocyte or after it is ovulated. This
is true, but only when, following ovulation of the mature
vitellogenic doublet, a single younger doublet develops in
the ovary after a period of no oogonial divisions. As a rule,
the ovary contains, besides oogonia, two pairs of oocytes –
the leading vitellogenic doublet and the succeeding previtellogenic doublet (see Table 1.7 ). The leading doublet occupies
most of the ovary, while the previtellogenic doublet is situated under it and generally a little to the side. This doublet
may appear in the ovary long before ovulation of the leader.
Silén’s assertion that growth of the second oocyte begins
only after oviposition of the fi rst one is also incorrect.
He observed the development of egg cells under a stereomicroscope, but could not see young primary oocytes, which
slowly begin to increase in size immediately after division of
the oogonium. Accelerated growth begins after ovulation of
the leading doublet. The main events of the sexual cycle are
rigidly synchronized; the next oocytes ripen by the time of
larval release from the ovicell. The idea that the development
of the embryo in the brood chamber and the growth of the
next oocyte in the ovary are hormonally synchronized was
fi rst suggested by Marcus ( 1938a ) and independently
expressed by Silén ( 1945 ).
It should be noted that, in some species (e.g. Cornucopina
polymorpha ), ovarian activity is synchronized at the level of
the colony – all oocytes in the studied colonies were at
the same stage of development. Judging from the size and
morphology of these cells, they were about to ovulate
(Fig. 1.11B ). Ovulation and larval development and release
are presumably synchronous too, which may be an important
feature of the ecological strategy of this species. The mechanism for this synchroneity appears to be hormonal (see also
Shunatova and Ostrovsky 2002 ).
According to Silén ( 1945 ), the average diameter of a coelomic oocyte in C . dumerilii is about 200 μm. Ryland
( 1976 ), citing the above-mentioned paper by Silén, gives a
value of 120 μm for the diameter of the late ovarian oocyte
(which agrees with my data) but no such fi gure can be found
in Silén’s text. According to Ryland ( 1976 , p. 361), the
oocyte grows to a diameter of 200 μm in the maternal coelom following ovulation. As discussed earlier, this increase
in size is possibly through water uptake. The discrepancy
between the latter value and my data on early embryo size in
this species (see Tables 1.6 ) may be explained by the fact
that Silén worked with live colonies, whereas I studied fi xed
material.
1.3.4.1 Vitellogenesis
Two factors infl uence the onset of vitellogenesis in cheilostome ovaries. (1) In a young ovary vitellogenesis starts only
after fertilization of one of the two oocytes in an early oocyte
doublet (Bishop et al. 2000 ; my data on Callopora lineata ,
see Sect. 1.2.4 ). (2) Later, in most cases, each succeeding
doublet starts to accumulate nutrient reserves only after
maturation and ovulation of the previous one. Because the
duration of previtellogenic growth may vary, vitellogenesis
may begin in oocytes of different age/size.
Normally, vitellogenesis begins in a zooid with an active
polypide. In most bryozoans the main bulk of nutrient
reserves is generated and accumulated in oocytes intrazooidally, that is, during the phase of active zooid feeding
(see Dyrynda and King 1983 ). On the other hand, the onset
of vitellogenesis is associated with non-regenerative polypide regression in the ctenostomes Alcyonidium diaphanum
and Bowerbankia gracilis while in the cheilostome Chartella
papyracea it is associated with the beginning of polypide
regeneration (see Chrétien 1958 ; Reed 1988 , 1991 ; Dyrynda
and Ryland 1982 ; Dyrynda and King 1983 ). The products of
polypide resorption are likely to be used for nutrition of the
oocyte (Ryland 1976 ; Reed 1991 ; my data on Callopora lineata and Corbulella maderensis ) or the embryo as in the
Epistomiidae (see Marcus 1941b ; Dyrynda and King 1982 ).
The fact that ovarian oocytes do not degenerate along with
the polypide but, instead, one of them starts to grow faster,
was reported as early as Joliet ( 1877 ) in the ctenostome
Walkeria uva . Indications that oogenesis continues during
polypide recycling can be found in the works of van
Beneden ( 1844b , in Alcyonidium sp.), Vigelius ( 1884b , in
Chartella membranaceotruncata ) and Pergens ( 1889 , in
Fenestrulina malusii ). Thus, in the absence of the feeding
polypide, oocyte development does not cease but continues
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
by the nurse cell (absent in Malacostegina), and yolk is
produced by the oocyte itself. The oocytes grow unequally,
with increase in size of the leading oocyte considerably
outstripping the nurse cell.
3. The fi nal (ovulatory) phase begins with partial degradation of the follicle wall. In malacostegans, contact (via
gap junctions) of the follicle cells with oocytes is lost
(Hageman 1983 ). Ovulation is a gradual process, in the
course of which the oocyte may remain in the ovary for
some time, partly exposed to the zooid cavity and sometimes continuing to accumulate reserve nutrients from the
coelomic fl uid by microvilli (Hughes 1987 ). The ovulatory phase is completed upon the release of the oocyte
from the ovary into the coelom, accompanied by degradation of the nurse cell, if any. It is during this phase that
fertilization occurs in malacostegans. The nuclear envelope degrades shortly before ovulation or soon after.
Silén’s ( 1945 ) landmark paper on sexual reproduction in
three bryozoan species with reproductive pattern II was a
major contribution to knowledge of oogenesis in cheilostome
brooders. Overall, the sequence of events is accurately
described in this study, but some observations and conclusions require comment. According to Silén, the ovary of
Callopora dumerilii contains a single oocyte [in fact, a doublet], with a second one appearing only at the fi nal developmental stage of the leading oocyte or after it is ovulated. This
is true, but only when, following ovulation of the mature
vitellogenic doublet, a single younger doublet develops in
the ovary after a period of no oogonial divisions. As a rule,
the ovary contains, besides oogonia, two pairs of oocytes –
the leading vitellogenic doublet and the succeeding previtellogenic doublet (see Table 1.7 ). The leading doublet occupies
most of the ovary, while the previtellogenic doublet is situated under it and generally a little to the side. This doublet
may appear in the ovary long before ovulation of the leader.
Silén’s assertion that growth of the second oocyte begins
only after oviposition of the fi rst one is also incorrect.
He observed the development of egg cells under a stereomicroscope, but could not see young primary oocytes, which
slowly begin to increase in size immediately after division of
the oogonium. Accelerated growth begins after ovulation of
the leading doublet. The main events of the sexual cycle are
rigidly synchronized; the next oocytes ripen by the time of
larval release from the ovicell. The idea that the development
of the embryo in the brood chamber and the growth of the
next oocyte in the ovary are hormonally synchronized was
fi rst suggested by Marcus ( 1938a ) and independently
expressed by Silén ( 1945 ).
It should be noted that, in some species (e.g. Cornucopina
polymorpha ), ovarian activity is synchronized at the level of
the colony – all oocytes in the studied colonies were at
the same stage of development. Judging from the size and
morphology of these cells, they were about to ovulate
(Fig. 1.11B ). Ovulation and larval development and release
are presumably synchronous too, which may be an important
feature of the ecological strategy of this species. The mechanism for this synchroneity appears to be hormonal (see also
Shunatova and Ostrovsky 2002 ).
According to Silén ( 1945 ), the average diameter of a coelomic oocyte in C . dumerilii is about 200 μm. Ryland
( 1976 ), citing the above-mentioned paper by Silén, gives a
value of 120 μm for the diameter of the late ovarian oocyte
(which agrees with my data) but no such fi gure can be found
in Silén’s text. According to Ryland ( 1976 , p. 361), the
oocyte grows to a diameter of 200 μm in the maternal coelom following ovulation. As discussed earlier, this increase
in size is possibly through water uptake. The discrepancy
between the latter value and my data on early embryo size in
this species (see Tables 1.6 ) may be explained by the fact
that Silén worked with live colonies, whereas I studied fi xed
material.
1.3.4.1 Vitellogenesis
Two factors infl uence the onset of vitellogenesis in cheilostome ovaries. (1) In a young ovary vitellogenesis starts only
after fertilization of one of the two oocytes in an early oocyte
doublet (Bishop et al. 2000 ; my data on Callopora lineata ,
see Sect. 1.2.4 ). (2) Later, in most cases, each succeeding
doublet starts to accumulate nutrient reserves only after
maturation and ovulation of the previous one. Because the
duration of previtellogenic growth may vary, vitellogenesis
may begin in oocytes of different age/size.
Normally, vitellogenesis begins in a zooid with an active
polypide. In most bryozoans the main bulk of nutrient
reserves is generated and accumulated in oocytes intrazooidally, that is, during the phase of active zooid feeding
(see Dyrynda and King 1983 ). On the other hand, the onset
of vitellogenesis is associated with non-regenerative polypide regression in the ctenostomes Alcyonidium diaphanum
and Bowerbankia gracilis while in the cheilostome Chartella
papyracea it is associated with the beginning of polypide
regeneration (see Chrétien 1958 ; Reed 1988 , 1991 ; Dyrynda
and Ryland 1982 ; Dyrynda and King 1983 ). The products of
polypide resorption are likely to be used for nutrition of the
oocyte (Ryland 1976 ; Reed 1991 ; my data on Callopora lineata and Corbulella maderensis ) or the embryo as in the
Epistomiidae (see Marcus 1941b ; Dyrynda and King 1982 ).
The fact that ovarian oocytes do not degenerate along with
the polypide but, instead, one of them starts to grow faster,
was reported as early as Joliet ( 1877 ) in the ctenostome
Walkeria uva . Indications that oogenesis continues during
polypide recycling can be found in the works of van
Beneden ( 1844b , in Alcyonidium sp.), Vigelius ( 1884b , in
Chartella membranaceotruncata ) and Pergens ( 1889 , in
Fenestrulina malusii ). Thus, in the absence of the feeding
polypide, oocyte development does not cease but continues
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata