61
sibling that fuses with the sperm becoming the vitellogenic
oocyte. Ryland and Bishop ( 1993 ) were the fi rst formally to
entertain this idea, but Dyrynda and King ( 1983 ) might have
anticipated this possibility when they observed that cells in
early doublets were distinguishable only by the presence of a
sperm head in one of them (see also Ostrovsky 1998 ). The
latter authors also demonstrated the presence of a “vitelline
envelope” in both ovarian oocytes and their nurse cells in
Chartella papyracea and Bugula fl abellata . It may be, therefore, that it is early syngamy and the change in the properties
of the cell membrane during the cortical reaction that brings
about the origin of oocyte doublets (see Sect. 3.2 ). Since the
cells of an oocyte doublet are connected by a cytoplasmic
bridge, the fusion of sperm with one of them might trigger a
spreading of the cortical reaction to both cells with the formation of a common precursor of a fertilization envelope,
thus preventing fertilization of the second cell.
Meiosis of the oocyte and the fusion of male and female
pronuclei are delayed until the removal of the oocyte from
the coelom of the maternal zooid (Ström 1977 ; Temkin 1994 ,
1996 ; my data). According to Temkin ( 1996 ), the activation
of the egg is also delayed, which may be associated with
preventing (1) cleavage from beginning inside the zooid, and
(2) the need for a very large egg to pass through a very small
genital pore. Descriptions and illustrations in some of the
early works (Vigelius 1884b ; Pergens 1889 ), and my own
data on Porella proboscidea , Mucropetraliella ellerii and
Petralia undata , indicate that, in some species at least, both
partly ovulated ovarian and ovulated coelomic oocytes possess a clearly visible fertilization envelope detached from the
oolemma. In contrast, ТЕМ studies by Dyrynda and King
( 1983 ), Hageman ( 1983 ) and Hughes ( 1987 ) showed the
presence of the “vitelline envelope” closely apposed to the
oolemma in both ovarian and coelomic oocytes. Thus, in the
former case, activation of a fertilized oocyte does occur but
is expressed only in the cortical reaction and detachment of
the fertilization envelope from the oolemma. In the second
case, it is not clear whether the cortical reaction is postponed
until egg release (despite syngamy) or actually takes place,
but the fertilization envelope is not yet detached. In both
cases the envelope seems extremely elastic and its presence
does not prevent oviposition/liberation of the oocyte from
the cavity of the maternal zooid. It is worth noting that, since
the fertilization envelope mostly becomes visible by light
microscopy only after oviposition or egg release, its appearance was often mistaken by researchers for the moment of
fertilization.
At the same time, in two species of viviparous cheilostomes (Epistomiidae) as well as in Cyclostomata, zygote
activation and embryo development occur in the coelom of
the maternal zooid. Cleavage sometimes starts, “by mistake”, in the coelom of other gymnolaemates, too. Barrois
( 1877 ) recorded two cleavage-stage embryos in the zooid
coelom of Membranipora sp. Gerwerzhagen ( 1913 ) once
observed a two-cell embryogenesis stage in the coelom of
the maternal zooid in Bugula avicularia . Developing
embryos were also seen in zooids of M. membranacea by
Lutaud ( 1961 ). Apparently, in these cases embryos could not
be released and fi nally degenerated.
As discussed above, the fertilization envelope becomes
noticeable by light microscopy in most species following
release of the mature oocyte from the zooid. In broadcasters
it ruptures after a few hours or a couple of days when the
young cyphonautes larva starts to feed (Cook 1962 ;
Mawatari 1975 ; see also Sect. 3.4.1 ). It disappears from late
embryos in brood chambers in some species (e.g. in Bugula
neritina , Celleporella hyalina and Costaticella spp.; see
Woollacott and Zimmer 1975 ; Hughes 1987 ; my data).
Since the latter species are characterized by placental
brooding, the destruction of the fertilization envelope might
be in some way connected with the uptake of nutrients from
brood-cavity fl uid by the embryo. In particular instances
(e.g. in Tegella , Menipea roborata and some others) the
fertilization envelope could not be detected by light microscopy, probably because it was too thin and/or very tightly
appressed to the embryonic surface. In some other cases, the
fertilization envelope is thick and, being retained in the
ovicell cavity following larval release ( Callopora lineata ,
C . dumerilii ), serves as evidence that the ovicell was used at
least once.
Temkin ( 1996 ) suggested that bryozoan ovaries, which
are a much larger target for sperm than oocytes, may release
sperm attractants. My data show that sperm penetrating into
the ovary are mostly located between the basal cells, in the
intraovarian space. Thus, insemination mostly occurs via the
intraovarian zone; it was only extremely rarely that sperm
heads were wedged between the tightly packed cells of the
ovary wall. The fi nding of numerous (up to 15) spermatozoids in the intraovarian space in many species indicates that
this part of the gonad functions as a seminal receptacle,
where the sperm may be stored for at least several weeks
(judging from the duration of ovary functioning) (see also
Sect. 1.2.1 ).
Once in the ovary, the sperm fuses with one of the cells of
the early oocyte doublet. The minimum size of the fertilized
oocyte recorded by Temkin ( 1996 ) was 34 μm (in Pacifi cincola
insculpta ). The youngest sperm-containing previtellogenic
oocytes observed by me were as small as 10 μm in diameter,
the sperm head being 8 μm long (in Tegella unicornis ). Owing
to limited space, the male pronuclei in the oocyte were
comma-shaped. This fi nding indicates that gametes must
have fused at the very end of oogonial mitosis. Further
research is necessary to determine if gametic fusion takes
place so early in all brooding cheilostomes. It is already clear,
however, that, in general, syngamy occurs even earlier than
Temkin ( 1996 ) thought.
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
sibling that fuses with the sperm becoming the vitellogenic
oocyte. Ryland and Bishop ( 1993 ) were the fi rst formally to
entertain this idea, but Dyrynda and King ( 1983 ) might have
anticipated this possibility when they observed that cells in
early doublets were distinguishable only by the presence of a
sperm head in one of them (see also Ostrovsky 1998 ). The
latter authors also demonstrated the presence of a “vitelline
envelope” in both ovarian oocytes and their nurse cells in
Chartella papyracea and Bugula fl abellata . It may be, therefore, that it is early syngamy and the change in the properties
of the cell membrane during the cortical reaction that brings
about the origin of oocyte doublets (see Sect. 3.2 ). Since the
cells of an oocyte doublet are connected by a cytoplasmic
bridge, the fusion of sperm with one of them might trigger a
spreading of the cortical reaction to both cells with the formation of a common precursor of a fertilization envelope,
thus preventing fertilization of the second cell.
Meiosis of the oocyte and the fusion of male and female
pronuclei are delayed until the removal of the oocyte from
the coelom of the maternal zooid (Ström 1977 ; Temkin 1994 ,
1996 ; my data). According to Temkin ( 1996 ), the activation
of the egg is also delayed, which may be associated with
preventing (1) cleavage from beginning inside the zooid, and
(2) the need for a very large egg to pass through a very small
genital pore. Descriptions and illustrations in some of the
early works (Vigelius 1884b ; Pergens 1889 ), and my own
data on Porella proboscidea , Mucropetraliella ellerii and
Petralia undata , indicate that, in some species at least, both
partly ovulated ovarian and ovulated coelomic oocytes possess a clearly visible fertilization envelope detached from the
oolemma. In contrast, ТЕМ studies by Dyrynda and King
( 1983 ), Hageman ( 1983 ) and Hughes ( 1987 ) showed the
presence of the “vitelline envelope” closely apposed to the
oolemma in both ovarian and coelomic oocytes. Thus, in the
former case, activation of a fertilized oocyte does occur but
is expressed only in the cortical reaction and detachment of
the fertilization envelope from the oolemma. In the second
case, it is not clear whether the cortical reaction is postponed
until egg release (despite syngamy) or actually takes place,
but the fertilization envelope is not yet detached. In both
cases the envelope seems extremely elastic and its presence
does not prevent oviposition/liberation of the oocyte from
the cavity of the maternal zooid. It is worth noting that, since
the fertilization envelope mostly becomes visible by light
microscopy only after oviposition or egg release, its appearance was often mistaken by researchers for the moment of
fertilization.
At the same time, in two species of viviparous cheilostomes (Epistomiidae) as well as in Cyclostomata, zygote
activation and embryo development occur in the coelom of
the maternal zooid. Cleavage sometimes starts, “by mistake”, in the coelom of other gymnolaemates, too. Barrois
( 1877 ) recorded two cleavage-stage embryos in the zooid
coelom of Membranipora sp. Gerwerzhagen ( 1913 ) once
observed a two-cell embryogenesis stage in the coelom of
the maternal zooid in Bugula avicularia . Developing
embryos were also seen in zooids of M. membranacea by
Lutaud ( 1961 ). Apparently, in these cases embryos could not
be released and fi nally degenerated.
As discussed above, the fertilization envelope becomes
noticeable by light microscopy in most species following
release of the mature oocyte from the zooid. In broadcasters
it ruptures after a few hours or a couple of days when the
young cyphonautes larva starts to feed (Cook 1962 ;
Mawatari 1975 ; see also Sect. 3.4.1 ). It disappears from late
embryos in brood chambers in some species (e.g. in Bugula
neritina , Celleporella hyalina and Costaticella spp.; see
Woollacott and Zimmer 1975 ; Hughes 1987 ; my data).
Since the latter species are characterized by placental
brooding, the destruction of the fertilization envelope might
be in some way connected with the uptake of nutrients from
brood-cavity fl uid by the embryo. In particular instances
(e.g. in Tegella , Menipea roborata and some others) the
fertilization envelope could not be detected by light microscopy, probably because it was too thin and/or very tightly
appressed to the embryonic surface. In some other cases, the
fertilization envelope is thick and, being retained in the
ovicell cavity following larval release ( Callopora lineata ,
C . dumerilii ), serves as evidence that the ovicell was used at
least once.
Temkin ( 1996 ) suggested that bryozoan ovaries, which
are a much larger target for sperm than oocytes, may release
sperm attractants. My data show that sperm penetrating into
the ovary are mostly located between the basal cells, in the
intraovarian space. Thus, insemination mostly occurs via the
intraovarian zone; it was only extremely rarely that sperm
heads were wedged between the tightly packed cells of the
ovary wall. The fi nding of numerous (up to 15) spermatozoids in the intraovarian space in many species indicates that
this part of the gonad functions as a seminal receptacle,
where the sperm may be stored for at least several weeks
(judging from the duration of ovary functioning) (see also
Sect. 1.2.1 ).
Once in the ovary, the sperm fuses with one of the cells of
the early oocyte doublet. The minimum size of the fertilized
oocyte recorded by Temkin ( 1996 ) was 34 μm (in Pacifi cincola
insculpta ). The youngest sperm-containing previtellogenic
oocytes observed by me were as small as 10 μm in diameter,
the sperm head being 8 μm long (in Tegella unicornis ). Owing
to limited space, the male pronuclei in the oocyte were
comma-shaped. This fi nding indicates that gametes must
have fused at the very end of oogonial mitosis. Further
research is necessary to determine if gametic fusion takes
place so early in all brooding cheilostomes. It is already clear,
however, that, in general, syngamy occurs even earlier than
Temkin ( 1996 ) thought.
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata