11
species of these genera, as well as the proximal position of
female zooids in respect to hermaphrodites, indicates that the
former were probably initially hermaphrodite, too, losing
spermatogenic tissue later. The colonies of these species thus
appear to be represented by sterile and hermaphroditic zooids
(variant 1). A similar situation is observed in Beania bilaminata , Amastigia cf. funiculata , and Steginoporella perplexa .
It should be emphasized once again that, in many
instances, information concerning sexual structure in cheilostome colonies is preliminary and should be carefully
checked. For example, in Steginoporella magnilabris
Harmer ( 1926 ) found both oocytes and sperm in А-zooids
(autozooids) and only spermatogenic tissue in В-zooids
(heteromorphic zooids). Thus, colonies of this species consisted of sterile, hermaphrodite and male zooids. I studied
colonies of what appeared to be the same species, which
consisted of sterile, male and (secondarily?) female zooids.
Studied colonies of S . perplexa were composed of sterile,
female and hermaphrodite zooids.
The predominantly proximal position of male zooids in
colonies, and, as a rule, the earlier development and degeneration of male gonads in hermaphrodite zooids, indicate
that most cheilostomes are either characterized by protandry
or have a protandrous phase preceding the phase of simultaneous hermaphroditism. Zooidal protogyny has been noted
in Cheilostomata only three times – in hermaphrodite zooids
of Chartella membranaceotruncata (see Vigelius 1882 ,
1884a , b ), in Bugula fl abellata (Dyrynda and Ryland
1982 ) and in Bicellariella ciliata (Moosbrugger et al. 2012 ;
see also Appendix I). Colonies of Hippoporina propinqua
studied by me consisted of sterile, hermaphrodite and male
autozooids, the latter being situated more distally. Since
spermatogenic tissue in hermaphrodite zooids was in the
early stages of maturation, it may be supposed that this
species is also protogynous.
The above examples show that a bryozoan colony is a
dynamic system, in which the gonads form, mature and
function at different times in different zooidal generations
(Ostrovsky 1998 , 2009 ). Reproductive activity of the zooids,
involving morphological specialization, is intimately associated with polypide recycling and seasonal changes in the life
of the colony, the latter correlating, in turn, with life cycle
and life span. Our knowledge of this aspect of bryozoan
biology is scarce in the extreme, and seasonal observations
are vitally important to reveal the sequence of sexual differentiation of zooids as well as whole colonies. For instance,
protandrous hermaphrodite colonies of Cribrilina annulata
are fi rst sterile and then male before becoming hermaphrodite. Taking into account the eventual degeneration of spermatogenic tissue in male and later hermaphrodite zooids, it
may be suggested that the colony then becomes female
(Ostrovsky 1998 ). In overwintering colonies of C. annulata , ovaries appear to degenerate, forming again at the
beginning of the next reproductive season in younger peripheral
zooids. If such is the case, colonies would be changing from
female to winter-sterile to protandrous-hermaphrodite again
in spring.
In Chartella papyracea , colonies are fi rst sterile, then
male, then hermaphrodite owing to successive formation of
male and female gonochoristic zooids. This sequence is
presumably infl uenced by temperature; towards winter the
colony becomes sterile again. Male gonads develop in many
female zooids (having ovicells but no ovaries) the following
spring (Dyrynda and Ryland 1982 ). Unfortunately, these
authors did not state whether new ovaries are formed in these
zooids or describe further changes in the sexual structure of
the colony.
In studying changes in the sexual structure of colonies,
one should also take into account differences in the duration
of the gonads relative to the life span of the polypide, zooid
and colony. Based on my own data and that in the literature,
female (sometimes also male) gonads are retained throughout the reproductive period in many species, to be inherited
by regenerated polypides (see, for instance, Dyrynda and
Ryland 1982 ). The ovary is inherited by the new polypide in
35 species studied (see Fig. 1.4C ). In Beania bilaminata , up
to two brown bodies were found in some fertile zooids, and
it is unlikely that an ovary is formed anew every time the
polypide regenerates. It is more probable that, once formed,
it functions during the lifetime of at least two polypides in
the same zooid, remaining functional in the intervening
period prior to inception of the second polypide (shown in
Chartella papyracea by Dyrynda and Ryland 1982 ).
Spermatogenic tissue, as a rule, degenerates before the
fi rst polypide recycling. For instance, Dyrynda and Ryland
( 1982 , p. 253) wrote that sperm release “takes place towards
the end of the polypide active life” in Bugula fl abellata.
However, I recorded in the latter species, as well as in Tegella
armifera , Cellaria fi stulosa (and possibly also in Antarctothoa
bougainvillei ), actively functioning spermatogenic tissue in
zooids with a brown body and a regenerating polypide.
Judging from the number of sperm, this tissue was formed or
began to form during the life of the fi rst polypide. Thus, in
some cheilostomes, sperm production continues after
polypide degeneration, anticipating regeneration of the new
polypide that is essential for release of sperm into the environment. In male zooids of Chartella papyracea , new spermatogenic tissue is formed each time the polypide regenerates
(Dyrynda and Ryland 1982 ).
Although a bryozoan colony lacks the centralization
inherent in unitary organisms, it reproduces as an integral
system, even though gametes are formed in numerous “separate” zooids. Synchronization of such events as maturation
and spawning of gametes demonstrates a high level of colonial integration. In some malacostegans, spawning of eggs
and sperm may be synchronized both within a colony and
1.2 Reproductive Patterns of Bryozoa
species of these genera, as well as the proximal position of
female zooids in respect to hermaphrodites, indicates that the
former were probably initially hermaphrodite, too, losing
spermatogenic tissue later. The colonies of these species thus
appear to be represented by sterile and hermaphroditic zooids
(variant 1). A similar situation is observed in Beania bilaminata , Amastigia cf. funiculata , and Steginoporella perplexa .
It should be emphasized once again that, in many
instances, information concerning sexual structure in cheilostome colonies is preliminary and should be carefully
checked. For example, in Steginoporella magnilabris
Harmer ( 1926 ) found both oocytes and sperm in А-zooids
(autozooids) and only spermatogenic tissue in В-zooids
(heteromorphic zooids). Thus, colonies of this species consisted of sterile, hermaphrodite and male zooids. I studied
colonies of what appeared to be the same species, which
consisted of sterile, male and (secondarily?) female zooids.
Studied colonies of S . perplexa were composed of sterile,
female and hermaphrodite zooids.
The predominantly proximal position of male zooids in
colonies, and, as a rule, the earlier development and degeneration of male gonads in hermaphrodite zooids, indicate
that most cheilostomes are either characterized by protandry
or have a protandrous phase preceding the phase of simultaneous hermaphroditism. Zooidal protogyny has been noted
in Cheilostomata only three times – in hermaphrodite zooids
of Chartella membranaceotruncata (see Vigelius 1882 ,
1884a , b ), in Bugula fl abellata (Dyrynda and Ryland
1982 ) and in Bicellariella ciliata (Moosbrugger et al. 2012 ;
see also Appendix I). Colonies of Hippoporina propinqua
studied by me consisted of sterile, hermaphrodite and male
autozooids, the latter being situated more distally. Since
spermatogenic tissue in hermaphrodite zooids was in the
early stages of maturation, it may be supposed that this
species is also protogynous.
The above examples show that a bryozoan colony is a
dynamic system, in which the gonads form, mature and
function at different times in different zooidal generations
(Ostrovsky 1998 , 2009 ). Reproductive activity of the zooids,
involving morphological specialization, is intimately associated with polypide recycling and seasonal changes in the life
of the colony, the latter correlating, in turn, with life cycle
and life span. Our knowledge of this aspect of bryozoan
biology is scarce in the extreme, and seasonal observations
are vitally important to reveal the sequence of sexual differentiation of zooids as well as whole colonies. For instance,
protandrous hermaphrodite colonies of Cribrilina annulata
are fi rst sterile and then male before becoming hermaphrodite. Taking into account the eventual degeneration of spermatogenic tissue in male and later hermaphrodite zooids, it
may be suggested that the colony then becomes female
(Ostrovsky 1998 ). In overwintering colonies of C. annulata , ovaries appear to degenerate, forming again at the
beginning of the next reproductive season in younger peripheral
zooids. If such is the case, colonies would be changing from
female to winter-sterile to protandrous-hermaphrodite again
in spring.
In Chartella papyracea , colonies are fi rst sterile, then
male, then hermaphrodite owing to successive formation of
male and female gonochoristic zooids. This sequence is
presumably infl uenced by temperature; towards winter the
colony becomes sterile again. Male gonads develop in many
female zooids (having ovicells but no ovaries) the following
spring (Dyrynda and Ryland 1982 ). Unfortunately, these
authors did not state whether new ovaries are formed in these
zooids or describe further changes in the sexual structure of
the colony.
In studying changes in the sexual structure of colonies,
one should also take into account differences in the duration
of the gonads relative to the life span of the polypide, zooid
and colony. Based on my own data and that in the literature,
female (sometimes also male) gonads are retained throughout the reproductive period in many species, to be inherited
by regenerated polypides (see, for instance, Dyrynda and
Ryland 1982 ). The ovary is inherited by the new polypide in
35 species studied (see Fig. 1.4C ). In Beania bilaminata , up
to two brown bodies were found in some fertile zooids, and
it is unlikely that an ovary is formed anew every time the
polypide regenerates. It is more probable that, once formed,
it functions during the lifetime of at least two polypides in
the same zooid, remaining functional in the intervening
period prior to inception of the second polypide (shown in
Chartella papyracea by Dyrynda and Ryland 1982 ).
Spermatogenic tissue, as a rule, degenerates before the
fi rst polypide recycling. For instance, Dyrynda and Ryland
( 1982 , p. 253) wrote that sperm release “takes place towards
the end of the polypide active life” in Bugula fl abellata.
However, I recorded in the latter species, as well as in Tegella
armifera , Cellaria fi stulosa (and possibly also in Antarctothoa
bougainvillei ), actively functioning spermatogenic tissue in
zooids with a brown body and a regenerating polypide.
Judging from the number of sperm, this tissue was formed or
began to form during the life of the fi rst polypide. Thus, in
some cheilostomes, sperm production continues after
polypide degeneration, anticipating regeneration of the new
polypide that is essential for release of sperm into the environment. In male zooids of Chartella papyracea , new spermatogenic tissue is formed each time the polypide regenerates
(Dyrynda and Ryland 1982 ).
Although a bryozoan colony lacks the centralization
inherent in unitary organisms, it reproduces as an integral
system, even though gametes are formed in numerous “separate” zooids. Synchronization of such events as maturation
and spawning of gametes demonstrates a high level of colonial integration. In some malacostegans, spawning of eggs
and sperm may be synchronized both within a colony and
1.2 Reproductive Patterns of Bryozoa