63
not see the actual female polypide in Celleporella hyalina , and
surmised that a tentacle sheath might have been involved in
the process, which led Levinsen ( 1909 ) to suggest that it took
place under a closed operculum (see above). The fi nding of
ascus parietal musculature in the female zooids of this species
(Ostrovsky 1998 ) indicates that transfer of the egg into the
ovicell may be an active process, involving inwards expansion
of the ascus, with concomitant increase in coelomic pressure,
forcing the oocyte out of the cavity of the maternal zooid into
the brood cavity via the presumed coelomopore (under the
closed operculum). In the same way, contraction of the parietal muscles would restore the original shape and position of
the ooecial vesicle in Scrupocellaria ferox (see Santagata
and Banta 1996 ). Such a mechanism, independent of the
polypide, could explain egg transfer in situations when the
polypide has regressed (see Pergens 1889 above).
Although the female zooid of C. hyalina has a rudimentary polypide, it is not actually known if is involved in oviposition. Hastings ( 1930 ) and Banta and Wass ( 1979 ) suggested
that its equivalent in Thalamoporella californica and catenicellids participates in oviposition. Nielsen ( 1981 ), on the other
hand, described oviposition under the operculum without
protrusion of the dwarf polypide in Pacifi cincola insculpta .
In this respect it is interesting to recall the observations of
Hastings ( 1932 ), who described some features of sexual
reproduction in Stylopoma informata and S . schizostoma ( S .
curvabile according to Tilbrook 2001 ). She reported that
fully formed peripheral zooids in S . informata can contain
mature sperm and, in some cases, a small ovary. Maternal
zooids, which initiate the formation of ovicells by distal
zooids, lack a polypide and have enlarged parietal muscles.
Hastings described three successive stages in oocyte development in such zooids in relation to events in the ovicell: (1)
the ovicell is empty but the ovary contains a large follicleenclosed “egg” [oocyte] and several small ones, (2) the ovicell
contains a large egg or embryo, while the ovary contains a
group of oocytes, most of which are rather larger than in state
(1), (3) the ovicell is empty, but the ovary may be in state 2
or one of the “eggs” may be enlarged and enclosed in a
follicle. Judging from this description, oviposition occurs
without the polypide in the egg-producing zooid. This is also
facilitated by a position of the zooid opening beneath the ovicell entrance (Hastings 1932 , text-fi g. 10).
In S . schizostoma , ovaries were noted in zooids near the
growing edge of the colony. Oocyte maturation and enlargement are accompanied by polypide degeneration. It is during
this period that ovicellogenesis begins. Hastings ( 1932 , p. 424)
stressed that “the degeneration of the polypide” coincides with
oocyte increase and ovicell formation, meaning that the products of its resorption can be utilized for the aforementioned
processes. She also thought that, since the “mature egg”
[leading oocyte doublet] occupies most of the zooid volume, the
polypide does not regenerate before completion of the ovicell
[since there is no space for the new polypide], which may
also indicate that the polypide is uninvolved in oviposition.
Nielsen ( 1981 ) described oviposition in Fenestrulina
miramara and Pacifi cincola insculpta . In the former it proceeds with the expanded polypide and the oocyte is slightly
deformed in the process, while in the latter it occurs under
the operculum without the expansion of the dwarf polypide.
The inheritance of preformed oocytes by a regenerated
polypide, as in Bugula avicularia and Chartella papyracea
(Gerwerzhagen 1913 ; Dyrynda and Ryland 1982 ), and their
subsequent transfer into the brood chamber, may also occur
in other species. Data indicating this possibility in cheilostomes with reproductive pattern II are given in Ostrovsky
( 1998 ). Marcus ( 1926a ) recorded mature eggs in zooids with
a degenerated polypide in Electra pilosa and suggested that
the oocytes should be spawned after its regeneration. In
contrast, the release of the mature larva in ovicell brooders
does not depend on any particular stage of polypide recycling, since the musculature of the ooecial vesicle and its
innervation are retained as cystid elements.
Finally, it should be noted that, whereas in some species
( Fenestrulina miramara ) up to three embryos are consecutively brooded without polypide degeneration (Nielsen
1981 ), in most cases observed ( Bugula foliolata , Watersipora
subtorquata , Bicellariella ciliata , Flustra foliacea ,
Chartella papyracea , Gontarella sp., Cupuladriidae), the
polypide degenerates some time after oviposition with subsequent regeneration for new ovipositional events (Corrêa
1948 ; Mawatari 1952 ; Eggleston 1972 ; Dyrynda 1981 ;
Dyrynda and Ryland 1982 ; Ostrovsky et al. 2006 , 2009c ).
On the other hand, it is also possible that polypide recycling
and brooding are not synchronized in some species
(e.g. “ Bifl ustra ” perfragilis , see Ostrovsky et al. 2006 ).
In Pacifi cincola insculpta, polypide recycling precedes
oviposition (Nielsen 1981 ), whereas in Epistomiidae and B .
pacifi ca , the polypide never regenerates (Marcus 1941b ;
Dyrynda 1981 ; Dyrynda and King 1982 ; Nielsen 1981 ).
1.3.8 Polymorphism in Reproductive Zooids
The origin of sexual zooidal polymorphism is associated
with the specialization of zooids for production, release and
dispersal of gametes, incubation of the embryos and possibly
the receipt of sperm. In its most extreme form, sexual polymorphism is expressed in the differences in zooid size associated with the housing of a large larva or the presence of a
reduced, non-feeding polypide (Cook 1973 , 1979 ; Silén 1977 ;
Reed 1991 ). Owing to the permanent or temporary presence
of a protrusible polypide (normal or specialized), reproductive zooids should be considered as autozooidal polymorphs
(Boardman et al. 1983 ). Silén ( 1977 , p. 208) termed both
“autozooidal and heterozooidal polymorphs specialized for
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
not see the actual female polypide in Celleporella hyalina , and
surmised that a tentacle sheath might have been involved in
the process, which led Levinsen ( 1909 ) to suggest that it took
place under a closed operculum (see above). The fi nding of
ascus parietal musculature in the female zooids of this species
(Ostrovsky 1998 ) indicates that transfer of the egg into the
ovicell may be an active process, involving inwards expansion
of the ascus, with concomitant increase in coelomic pressure,
forcing the oocyte out of the cavity of the maternal zooid into
the brood cavity via the presumed coelomopore (under the
closed operculum). In the same way, contraction of the parietal muscles would restore the original shape and position of
the ooecial vesicle in Scrupocellaria ferox (see Santagata
and Banta 1996 ). Such a mechanism, independent of the
polypide, could explain egg transfer in situations when the
polypide has regressed (see Pergens 1889 above).
Although the female zooid of C. hyalina has a rudimentary polypide, it is not actually known if is involved in oviposition. Hastings ( 1930 ) and Banta and Wass ( 1979 ) suggested
that its equivalent in Thalamoporella californica and catenicellids participates in oviposition. Nielsen ( 1981 ), on the other
hand, described oviposition under the operculum without
protrusion of the dwarf polypide in Pacifi cincola insculpta .
In this respect it is interesting to recall the observations of
Hastings ( 1932 ), who described some features of sexual
reproduction in Stylopoma informata and S . schizostoma ( S .
curvabile according to Tilbrook 2001 ). She reported that
fully formed peripheral zooids in S . informata can contain
mature sperm and, in some cases, a small ovary. Maternal
zooids, which initiate the formation of ovicells by distal
zooids, lack a polypide and have enlarged parietal muscles.
Hastings described three successive stages in oocyte development in such zooids in relation to events in the ovicell: (1)
the ovicell is empty but the ovary contains a large follicleenclosed “egg” [oocyte] and several small ones, (2) the ovicell
contains a large egg or embryo, while the ovary contains a
group of oocytes, most of which are rather larger than in state
(1), (3) the ovicell is empty, but the ovary may be in state 2
or one of the “eggs” may be enlarged and enclosed in a
follicle. Judging from this description, oviposition occurs
without the polypide in the egg-producing zooid. This is also
facilitated by a position of the zooid opening beneath the ovicell entrance (Hastings 1932 , text-fi g. 10).
In S . schizostoma , ovaries were noted in zooids near the
growing edge of the colony. Oocyte maturation and enlargement are accompanied by polypide degeneration. It is during
this period that ovicellogenesis begins. Hastings ( 1932 , p. 424)
stressed that “the degeneration of the polypide” coincides with
oocyte increase and ovicell formation, meaning that the products of its resorption can be utilized for the aforementioned
processes. She also thought that, since the “mature egg”
[leading oocyte doublet] occupies most of the zooid volume, the
polypide does not regenerate before completion of the ovicell
[since there is no space for the new polypide], which may
also indicate that the polypide is uninvolved in oviposition.
Nielsen ( 1981 ) described oviposition in Fenestrulina
miramara and Pacifi cincola insculpta . In the former it proceeds with the expanded polypide and the oocyte is slightly
deformed in the process, while in the latter it occurs under
the operculum without the expansion of the dwarf polypide.
The inheritance of preformed oocytes by a regenerated
polypide, as in Bugula avicularia and Chartella papyracea
(Gerwerzhagen 1913 ; Dyrynda and Ryland 1982 ), and their
subsequent transfer into the brood chamber, may also occur
in other species. Data indicating this possibility in cheilostomes with reproductive pattern II are given in Ostrovsky
( 1998 ). Marcus ( 1926a ) recorded mature eggs in zooids with
a degenerated polypide in Electra pilosa and suggested that
the oocytes should be spawned after its regeneration. In
contrast, the release of the mature larva in ovicell brooders
does not depend on any particular stage of polypide recycling, since the musculature of the ooecial vesicle and its
innervation are retained as cystid elements.
Finally, it should be noted that, whereas in some species
( Fenestrulina miramara ) up to three embryos are consecutively brooded without polypide degeneration (Nielsen
1981 ), in most cases observed ( Bugula foliolata , Watersipora
subtorquata , Bicellariella ciliata , Flustra foliacea ,
Chartella papyracea , Gontarella sp., Cupuladriidae), the
polypide degenerates some time after oviposition with subsequent regeneration for new ovipositional events (Corrêa
1948 ; Mawatari 1952 ; Eggleston 1972 ; Dyrynda 1981 ;
Dyrynda and Ryland 1982 ; Ostrovsky et al. 2006 , 2009c ).
On the other hand, it is also possible that polypide recycling
and brooding are not synchronized in some species
(e.g. “ Bifl ustra ” perfragilis , see Ostrovsky et al. 2006 ).
In Pacifi cincola insculpta, polypide recycling precedes
oviposition (Nielsen 1981 ), whereas in Epistomiidae and B .
pacifi ca , the polypide never regenerates (Marcus 1941b ;
Dyrynda 1981 ; Dyrynda and King 1982 ; Nielsen 1981 ).
1.3.8 Polymorphism in Reproductive Zooids
The origin of sexual zooidal polymorphism is associated
with the specialization of zooids for production, release and
dispersal of gametes, incubation of the embryos and possibly
the receipt of sperm. In its most extreme form, sexual polymorphism is expressed in the differences in zooid size associated with the housing of a large larva or the presence of a
reduced, non-feeding polypide (Cook 1973 , 1979 ; Silén 1977 ;
Reed 1991 ). Owing to the permanent or temporary presence
of a protrusible polypide (normal or specialized), reproductive zooids should be considered as autozooidal polymorphs
(Boardman et al. 1983 ). Silén ( 1977 , p. 208) termed both
“autozooidal and heterozooidal polymorphs specialized for
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata