60
Marcus ( 1938a , 1941a ), who observed male pronuclei in
previtellogenic oocytes in several cheilostomes. Based on this
discovery, he concluded that at least some bryozoan species
have cross- fertilization. For example, only alien sperm can
be contained in the ovary in cases of protogyny as well as in
the colonies with gonochoristic female zooids. At the same
time, protandric hermaphroditism does not necessarily mean
that the organism should cross-fertilize. Self-fertilization is
theoretically possible in this case, too, since early oocytes
are fertilized. The third important implication of the discovery of precocious fertilization was that simultaneous hermaphroditism cannot be taken as evidence of intrazooidal
self- fertilization, since early oocytes may be fertilized only
by mature, and thus alien, sperm (Marcus 1938a ).
Somewhat later, Silén ( 1944 ) found sperm heads in ovulated oocytes of the protogynous ctenostome Labiostomella
gisleni , Corrêa ( 1948 ) described sperm-containing early
oocytes in the ovaries of Bugula foliolata and Mawatari
( 1952 ) reported a similar fi nding in developing oocytes of
Watersipora subtorquata . Sperm were also found in several
large ovarian oocytes in Selenaria maculata (Chimonides
and Cook 1981 ). Dyrynda and King ( 1983 ) described sperm
in previtellogenic and vitellogenic oocytes of Chartella papyracea . Hughes ( 1987 ) observed a sperm head between ovarian cells in Celleporella hyalina .
Despite the fi ndings of Marcus ( 1938a , 1941a), and also
Cori ( 1941 ) who depicted sperm in the tentacle coelom of
the ctenostome Zoobotryon verticillatum , plus Brien’s
( 1960 ) suggestion that sperm might be released via terminal
tentacular pores, the notion of intrazooidal self-fertilization
in Bryozoa has persisted into the early twenty-fi rst century
(see Smith et al. 2003 ). The major turning point was the
study by Silén ( 1966 ), who observed sperm release in four
malacostegine species (see Sects. 1.1 and 1.2.1 ), thereby
providing conclusive evidence for cross-fertilization. As for
fusion of gametes, Silén’s conclusions were as follows: in E .
posidoniae it happens in the environment (judging from the
appearance of the fertilization envelope, until recently used
as the basic indicator of fertilization), while in Einhornia
crustulenta it happens in the cavity of the intertentacular
organ (inside which sperm were found). Returning to the old
idea of Joliet ( 1877 ), Silén ( 1966 ) suggested that, in brooders, male and female gametes may fuse outside zooidal
coelom. Strangely enough, he seems to have ignored the
fi ndings of the early fertilization by Marcus ( 1938a ) in
various brooding gymnolaemates though he referred to the
latter study. On the other hand, Silén indicated that, since
sperm could theoretically enter the zooid cavity via the
supraneural pore or intertentacular organ, fertilization might
also be internal, in accord with his own conclusion about
post-ovulatory intracoelomic fertilization in Callopora
dumerilii (see Silén 1945 ). Meanwhile, Prouho ( 1892 )
thought it impossible for the intertentacular organ to be used
for the transfer of sperm to the zooid cavity, since its ciliary
beat is directed outwards.
Temkin ( 1994 , 1996 ) should be credited with the defi nitive clarifi cation of this issue. He studied eight cheilostome
and two ctenostome species; in all of them fertilization was
shown to be internal. In Membranipora membranacea
sperm clusters (spermatozeugmata) are released via the
terminal pores of two dorso-medial tentacles tail first.
The free- swimming period ends differently – some spermatozeugmata are carried out of the colony, some are swallowed, and, among those that have adhered to the tentacles
of other zooids, only a few reach the opening of the intertentacular organ, the others becoming entangled between the
cilia. The intertentacular organ (Fig. 1.1C ) actively regulates the entrance of sperm into the zooid by opening and
closing. Notwithstanding, it cannot distinguish between its
own sperm (formed in the same colony) and allosperm. A
sperm fuses with a mature oocyte either during ovulation or
shortly after it. The nuclear membrane collapses at about the
same time. In one instance, 14 male pronuclei were found in
an oocyte, indicating the possibility of polyspermy (see
Bonnevie 1907 , and the discussion above). Zygote activation (accompanied by the acquisition of a rounded shape
and separation of the fertilization envelope), the formation
of polar bodies and karyogamy are delayed until after
spawning. This delay appears to be a necessary condition
for passage of the oocyte via the narrow lumen of the intertentacular organ.
Thus, in broadcasters, the sperm fuses with the oocyte at
or near ovulation, i.e. while the oocyte is still in the ovary
(in the process of release into the cavity of the fertile zooid)
or ovulated. Besides M. membranacea , this variant of fertilization occurs in a species of Alcyonidium , containing up to
60 small intra-ovarian oocytes, and Electra pilosa (Temkin
1996 ). Marcus ( 1938a , p. 119) found sperm in oocytes “in
the beginning of their second growing period” [presumably
vitellogenesis] in Alcyonidium mamillatum , a known broadcaster (Porter, personal communication, 2010), but Marcus’s
specimen may have been misidentifi ed since it was described
as lacking the intertentacular organ characteristic of broadcasters (see Ostrovsky and Porter 2011 ).
In brooding bryozoans, fertilization always occurs in the
ovary. For example, the sperm fuses with a late-stage ovarian
oocyte in the brooding ctenostome Bowerbankia gracilis
before degradation of its nuclear envelope. A single fertilized
oocyte is contained in the ovary, and syngamy appears to
be possible owing to rupture of the follicle and partial ovulation
of the oocyte (discussed in Temkin 1996 ). Marcus ( 1938a )
found sperm in a “growing” oocyte in Nolella stipata . In all
other gymnolaemates studied, sperm fuse with early ovarian
oocytes.
Cellular differentiation in an early oocyte doublet is
presumably determined by the fertilization “address”, the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
Marcus ( 1938a , 1941a ), who observed male pronuclei in
previtellogenic oocytes in several cheilostomes. Based on this
discovery, he concluded that at least some bryozoan species
have cross- fertilization. For example, only alien sperm can
be contained in the ovary in cases of protogyny as well as in
the colonies with gonochoristic female zooids. At the same
time, protandric hermaphroditism does not necessarily mean
that the organism should cross-fertilize. Self-fertilization is
theoretically possible in this case, too, since early oocytes
are fertilized. The third important implication of the discovery of precocious fertilization was that simultaneous hermaphroditism cannot be taken as evidence of intrazooidal
self- fertilization, since early oocytes may be fertilized only
by mature, and thus alien, sperm (Marcus 1938a ).
Somewhat later, Silén ( 1944 ) found sperm heads in ovulated oocytes of the protogynous ctenostome Labiostomella
gisleni , Corrêa ( 1948 ) described sperm-containing early
oocytes in the ovaries of Bugula foliolata and Mawatari
( 1952 ) reported a similar fi nding in developing oocytes of
Watersipora subtorquata . Sperm were also found in several
large ovarian oocytes in Selenaria maculata (Chimonides
and Cook 1981 ). Dyrynda and King ( 1983 ) described sperm
in previtellogenic and vitellogenic oocytes of Chartella papyracea . Hughes ( 1987 ) observed a sperm head between ovarian cells in Celleporella hyalina .
Despite the fi ndings of Marcus ( 1938a , 1941a), and also
Cori ( 1941 ) who depicted sperm in the tentacle coelom of
the ctenostome Zoobotryon verticillatum , plus Brien’s
( 1960 ) suggestion that sperm might be released via terminal
tentacular pores, the notion of intrazooidal self-fertilization
in Bryozoa has persisted into the early twenty-fi rst century
(see Smith et al. 2003 ). The major turning point was the
study by Silén ( 1966 ), who observed sperm release in four
malacostegine species (see Sects. 1.1 and 1.2.1 ), thereby
providing conclusive evidence for cross-fertilization. As for
fusion of gametes, Silén’s conclusions were as follows: in E .
posidoniae it happens in the environment (judging from the
appearance of the fertilization envelope, until recently used
as the basic indicator of fertilization), while in Einhornia
crustulenta it happens in the cavity of the intertentacular
organ (inside which sperm were found). Returning to the old
idea of Joliet ( 1877 ), Silén ( 1966 ) suggested that, in brooders, male and female gametes may fuse outside zooidal
coelom. Strangely enough, he seems to have ignored the
fi ndings of the early fertilization by Marcus ( 1938a ) in
various brooding gymnolaemates though he referred to the
latter study. On the other hand, Silén indicated that, since
sperm could theoretically enter the zooid cavity via the
supraneural pore or intertentacular organ, fertilization might
also be internal, in accord with his own conclusion about
post-ovulatory intracoelomic fertilization in Callopora
dumerilii (see Silén 1945 ). Meanwhile, Prouho ( 1892 )
thought it impossible for the intertentacular organ to be used
for the transfer of sperm to the zooid cavity, since its ciliary
beat is directed outwards.
Temkin ( 1994 , 1996 ) should be credited with the defi nitive clarifi cation of this issue. He studied eight cheilostome
and two ctenostome species; in all of them fertilization was
shown to be internal. In Membranipora membranacea
sperm clusters (spermatozeugmata) are released via the
terminal pores of two dorso-medial tentacles tail first.
The free- swimming period ends differently – some spermatozeugmata are carried out of the colony, some are swallowed, and, among those that have adhered to the tentacles
of other zooids, only a few reach the opening of the intertentacular organ, the others becoming entangled between the
cilia. The intertentacular organ (Fig. 1.1C ) actively regulates the entrance of sperm into the zooid by opening and
closing. Notwithstanding, it cannot distinguish between its
own sperm (formed in the same colony) and allosperm. A
sperm fuses with a mature oocyte either during ovulation or
shortly after it. The nuclear membrane collapses at about the
same time. In one instance, 14 male pronuclei were found in
an oocyte, indicating the possibility of polyspermy (see
Bonnevie 1907 , and the discussion above). Zygote activation (accompanied by the acquisition of a rounded shape
and separation of the fertilization envelope), the formation
of polar bodies and karyogamy are delayed until after
spawning. This delay appears to be a necessary condition
for passage of the oocyte via the narrow lumen of the intertentacular organ.
Thus, in broadcasters, the sperm fuses with the oocyte at
or near ovulation, i.e. while the oocyte is still in the ovary
(in the process of release into the cavity of the fertile zooid)
or ovulated. Besides M. membranacea , this variant of fertilization occurs in a species of Alcyonidium , containing up to
60 small intra-ovarian oocytes, and Electra pilosa (Temkin
1996 ). Marcus ( 1938a , p. 119) found sperm in oocytes “in
the beginning of their second growing period” [presumably
vitellogenesis] in Alcyonidium mamillatum , a known broadcaster (Porter, personal communication, 2010), but Marcus’s
specimen may have been misidentifi ed since it was described
as lacking the intertentacular organ characteristic of broadcasters (see Ostrovsky and Porter 2011 ).
In brooding bryozoans, fertilization always occurs in the
ovary. For example, the sperm fuses with a late-stage ovarian
oocyte in the brooding ctenostome Bowerbankia gracilis
before degradation of its nuclear envelope. A single fertilized
oocyte is contained in the ovary, and syngamy appears to
be possible owing to rupture of the follicle and partial ovulation
of the oocyte (discussed in Temkin 1996 ). Marcus ( 1938a )
found sperm in a “growing” oocyte in Nolella stipata . In all
other gymnolaemates studied, sperm fuse with early ovarian
oocytes.
Cellular differentiation in an early oocyte doublet is
presumably determined by the fertilization “address”, the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis