10
maturation of male and female gonads in hermaphrodite
zooids. The same combination of zooids was described in
C . membranaceotruncata by Vigelius ( 1882 , 1884a , b ) and
in “C.” indivisa by Stach ( 1938 ). The simultaneous presence
of three “types” of sexual zooids in the same colony led
Vigelius to conclude that, depending on conditions, female
zooids might transform into hermaphrodites and then back to
females (see Appendix I). Thus, the variant under discussion
is possible if colonies consist of sterile, male and sequentially hermaphrodite zooids with a protogynous phase
(they initially are females, but later become simultaneous
hermaphrodites). However, the aforementioned sexual
structure is also theoretically possible when a colony
consists of (a) sterile, male and hermaphrodite zooids with
a protandrous phase (the latter start as males, change to
simultaneous hermaphrodites, and then to females after
degradation of spermatogenic tissue), and (b) sterile, male,
female and hermaphrodite zooids.
Presumably the simplest variant, 1, is commonest, but seasonal observations are required for confi rmation. For instance,
Bonnevie ( 1907 ) wrote that, throughout the entire reproductive
season, colonies of Electra pilosa and Membranipora membranacea included male, female and hermaphrodite zooids, but
they were all, in fact, hermaphrodites in different stages of
gonad formation and functioning. Bonnevie suggested that
some zooids were possibly protandrous hermaphrodites, but
did not exclude the possibility that different gonads could
repeatedly originate during the life span of the same zooid.
In hermaphrodite zooids of Membranipora serrilamella ,
ovaries are always formed later than testes, with male and
female reproductive phases either somewhat overlapping or
separated by a time gap (Hageman 1983 ). In mature colonies, there is a peripheral zone of young zooids without
gonads, a subperipheral zone of zooids in which testes are
developing (situated among sterile ones) and a more inner
zone (or several belt zones) consisting of simultaneously
hermaphrodite (and sterile) zooids; fi nally, the colony centre
is represented by the oldest zooids with degenerated polypides without gonads.
According to Cancino et al. ( 1991 ), distinct protandrous
zooidal hermaphroditism is characteristic of Membranipora
isabelleana . Mature oocytes and sperm were never found in
the zooidal cavity at the same time, with colonies consisting
of sterile, “male” and “female” zooids. The true sexual structure of M . isabelleana colonies could be revealed only by
prolonged observations of colonies kept in aquaria. Thus, in
this case we deal not with variant 2 of sexual structure but
with variant 1. However, in most species gonad development
and function in hermaphrodite zooids overlap. Depending on
which gonad starts to develop fi rst, the protandrous or protogynous phase of zooidal sexual development begins, further changing to a phase of simultaneous hermaphroditism,
often returning to a monosexual phase again.
Variant 2, i.e. co-occurrence of sterile and gonochoristic
(male and female) zooids, is described in the literature for
about 10 species, and I have found 25 additional species in
the course of my research (see Table 1.1 ). Thus, this variant
of sexual structure is also rather common. In some species,
gonochoristic zooids are characterized by sexual dimorphism
expressed in the modifi cation of the cystid, the polypide or
both (see Sect. 1.3.8 ).
Variant 3 of sexual structure (co-occurrence of sterile,
male and hermaphrodite zooids) was fi rst reported by Silén
( 1966 ), who noted that in Electra posidoniae colonies, which
were most of the time represented by sterile and hermaphrodite zooids, male zooids appeared towards the end of reproduction. Interestingly, although hermaphrodite zooids are
typically protandrous in this species, simultaneous maturation of both eggs and sperm may also occur in some zooids.
I found male gonochoristic and hermaphrodite zooids in
colonies of Cribrilina annulata [judging from their proximal
position, males developed earlier than hermaphrodites
(Ostrovsky 1998 )] and later observed this variant of sexual
structure in 23 other species (see Table 1.1 ).
I have also observed species whose colonies consisted of
sterile, female and hermaphrodite zooids (Ostrovsky 2009 ).
For instance, peripheral female zooids in the colonies of
Callopora lineata and Cauloramphus spinifer had no traces
of male gametes at the time of collection. Female zooids were
also found at the periphery of Smittina antarctica colonies.
However, we cannot be sure whether these zooids are gonochoristic, or protogynous hermaphrodites in which spermatogenic tissue is not yet formed until seasonal observations
are made. As noted above, delay in the formation of male and
female gonads in hermaphrodite zooids may be considerable,
ranging from 2 to 3 days in Electra posidoniae up to 8–10 days
in Membranipora isabelleana (see Silén 1966 ; Cancino et al.
1991 ). In C . spinifer , female zooids were found both more
distally and more proximally than hermaphrodites. In most
studied species with hermaphrodite zooids, spermatogenic
tissue is “spent” rather fast. Therefore, if we suppose that all
sexual zooids in colonies of C . spinifer are hermaphrodites in
which the ovary develops earlier than male gonad (protogynous phase), then spermatogenic tissue should already be
lacking in the proximal “females”, developing/functioning
actively in the more distal hermaphrodite zooids (phase of
simultaneous hermaphroditism) while not yet formed in the
distalmost ones. The presence of distal female zooids is also
possible if this species is characterized by hermaphroditism
with a protandrous phase and female gonochorism. In this
case, spermatogenic tissue is already lacking in the proximal
“female” zooids and present in the more distal hermaphrodite
zooids, while in the distalmost ones it is never formed.
Sterile, female and hermaphrodite zooids were also found
to constitute colonies of Rhamphostomella bilaminata and
Turbicellepora crenulata . Colonial sexual structure in other
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
maturation of male and female gonads in hermaphrodite
zooids. The same combination of zooids was described in
C . membranaceotruncata by Vigelius ( 1882 , 1884a , b ) and
in “C.” indivisa by Stach ( 1938 ). The simultaneous presence
of three “types” of sexual zooids in the same colony led
Vigelius to conclude that, depending on conditions, female
zooids might transform into hermaphrodites and then back to
females (see Appendix I). Thus, the variant under discussion
is possible if colonies consist of sterile, male and sequentially hermaphrodite zooids with a protogynous phase
(they initially are females, but later become simultaneous
hermaphrodites). However, the aforementioned sexual
structure is also theoretically possible when a colony
consists of (a) sterile, male and hermaphrodite zooids with
a protandrous phase (the latter start as males, change to
simultaneous hermaphrodites, and then to females after
degradation of spermatogenic tissue), and (b) sterile, male,
female and hermaphrodite zooids.
Presumably the simplest variant, 1, is commonest, but seasonal observations are required for confi rmation. For instance,
Bonnevie ( 1907 ) wrote that, throughout the entire reproductive
season, colonies of Electra pilosa and Membranipora membranacea included male, female and hermaphrodite zooids, but
they were all, in fact, hermaphrodites in different stages of
gonad formation and functioning. Bonnevie suggested that
some zooids were possibly protandrous hermaphrodites, but
did not exclude the possibility that different gonads could
repeatedly originate during the life span of the same zooid.
In hermaphrodite zooids of Membranipora serrilamella ,
ovaries are always formed later than testes, with male and
female reproductive phases either somewhat overlapping or
separated by a time gap (Hageman 1983 ). In mature colonies, there is a peripheral zone of young zooids without
gonads, a subperipheral zone of zooids in which testes are
developing (situated among sterile ones) and a more inner
zone (or several belt zones) consisting of simultaneously
hermaphrodite (and sterile) zooids; fi nally, the colony centre
is represented by the oldest zooids with degenerated polypides without gonads.
According to Cancino et al. ( 1991 ), distinct protandrous
zooidal hermaphroditism is characteristic of Membranipora
isabelleana . Mature oocytes and sperm were never found in
the zooidal cavity at the same time, with colonies consisting
of sterile, “male” and “female” zooids. The true sexual structure of M . isabelleana colonies could be revealed only by
prolonged observations of colonies kept in aquaria. Thus, in
this case we deal not with variant 2 of sexual structure but
with variant 1. However, in most species gonad development
and function in hermaphrodite zooids overlap. Depending on
which gonad starts to develop fi rst, the protandrous or protogynous phase of zooidal sexual development begins, further changing to a phase of simultaneous hermaphroditism,
often returning to a monosexual phase again.
Variant 2, i.e. co-occurrence of sterile and gonochoristic
(male and female) zooids, is described in the literature for
about 10 species, and I have found 25 additional species in
the course of my research (see Table 1.1 ). Thus, this variant
of sexual structure is also rather common. In some species,
gonochoristic zooids are characterized by sexual dimorphism
expressed in the modifi cation of the cystid, the polypide or
both (see Sect. 1.3.8 ).
Variant 3 of sexual structure (co-occurrence of sterile,
male and hermaphrodite zooids) was fi rst reported by Silén
( 1966 ), who noted that in Electra posidoniae colonies, which
were most of the time represented by sterile and hermaphrodite zooids, male zooids appeared towards the end of reproduction. Interestingly, although hermaphrodite zooids are
typically protandrous in this species, simultaneous maturation of both eggs and sperm may also occur in some zooids.
I found male gonochoristic and hermaphrodite zooids in
colonies of Cribrilina annulata [judging from their proximal
position, males developed earlier than hermaphrodites
(Ostrovsky 1998 )] and later observed this variant of sexual
structure in 23 other species (see Table 1.1 ).
I have also observed species whose colonies consisted of
sterile, female and hermaphrodite zooids (Ostrovsky 2009 ).
For instance, peripheral female zooids in the colonies of
Callopora lineata and Cauloramphus spinifer had no traces
of male gametes at the time of collection. Female zooids were
also found at the periphery of Smittina antarctica colonies.
However, we cannot be sure whether these zooids are gonochoristic, or protogynous hermaphrodites in which spermatogenic tissue is not yet formed until seasonal observations
are made. As noted above, delay in the formation of male and
female gonads in hermaphrodite zooids may be considerable,
ranging from 2 to 3 days in Electra posidoniae up to 8–10 days
in Membranipora isabelleana (see Silén 1966 ; Cancino et al.
1991 ). In C . spinifer , female zooids were found both more
distally and more proximally than hermaphrodites. In most
studied species with hermaphrodite zooids, spermatogenic
tissue is “spent” rather fast. Therefore, if we suppose that all
sexual zooids in colonies of C . spinifer are hermaphrodites in
which the ovary develops earlier than male gonad (protogynous phase), then spermatogenic tissue should already be
lacking in the proximal “females”, developing/functioning
actively in the more distal hermaphrodite zooids (phase of
simultaneous hermaphroditism) while not yet formed in the
distalmost ones. The presence of distal female zooids is also
possible if this species is characterized by hermaphroditism
with a protandrous phase and female gonochorism. In this
case, spermatogenic tissue is already lacking in the proximal
“female” zooids and present in the more distal hermaphrodite
zooids, while in the distalmost ones it is never formed.
Sterile, female and hermaphrodite zooids were also found
to constitute colonies of Rhamphostomella bilaminata and
Turbicellepora crenulata . Colonial sexual structure in other
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis