68
ctenostome Zoobotryon verticillatum , but Silén did not
mention this fi nding. It should be stressed that, despite Silen’s
assumption, there is no evidence to date that the terminal
pores of tentacles were ever used by bryozoans as a conduit
for the entry of sperm. In some phoronids, however, the sperm
lyses through tentacle walls (Zimmer 1991 ).
Twenty years later it was discovered by Silén himself that
tentacles are male gonoducts in Bryozoa (Silén 1966 , 1972 ; see
also Bullivant 1967 ; Temkin 1994 ). In general, Silén’s speculations concerning the evolution of brooding, oviposition and
larval types in Gymnolaemata are highly disputable (criticized by Santagata and Banta 1996 and Ostrovsky 2009 ),
and were often based on wrongly interpreted facts. For instance,
his suggestion concerning the formation of the abovementioned “embryonary” (and thus speculations about egg release)
in ctenostomes is wrong since eggs immerse in the body wall
after their release (reviewed in Ström 1977 , see also Sect. 3.1.1 ).
According to the second hypothesis, the earliest Bryozoa
had a female gonopore (SNP) originally used both for spawning and for the entry of alien sperm, whereas terminal (coelomo)pores of the tentacles served as male gonopores for sperm
release. The ITO evolved later as an extension of the female
gonopore, retaining its functions (Ostrovsky and Porter 2011 ).
The difference between the two hypotheses on the origin
of the ITO is that in the fi rst case it supposedly evolved by
fusion of two entire dorso-medial tentacles, accompanied by
shortening and functional modifi cation (as a conduit for egg
release and sperm entry), while in the other, the ITO is
formed by the fusion of the basal parts of two dorso-medial
tentacles and did not change its function. In the fi rst case, the
terminal pore of the ITO corresponds to the male gonopore,
whereas in the second it is originated from the female one.
1.3.9.2 Origin of the Supraneural Coelomopore
Broadcasting is generally considered to be an ancestral
reproductive pattern in marine invertebrates (Jägersten 1972 ;
Levin and Bridges 1995 ; Havenhand 1995 ), including bryozoans (Zimmer and Woollacott 1977 ; Strathmann 1978 ;
Taylor 1988 ). In agreement with this idea, Reed ( 1991 ) stated
that the presence of an ITO is a primitive condition.
Ostrovsky and Porter ( 2011 ) agreed that the ITO evolved
early in the Bryozoa in broadcasting ctenostomes and cheilostomes. Nevertheless, they suggested that the initial state of
this character was a simple female gonopore that served for
both sperm entry and spawning in the earliest bryozoans. In
Phylactolaemata, a coelomopore in a vestibular wall through
which statoblasts, and, incidentally, sperm are released, has
been recorded by Marcus ( 1941a , 1942 ) and Wiebach ( 1953 ).
The position of this pore below the anus, at duplicature (i.e. at
the cystid wall) and not at the lophophore base, questions its
homology with the SNP in gymnolaemates (see also Marcus
1941a ). It may serve as a route for alien sperm. At the same
time, it is not known if it is used for oviposition. According
to Brien ( 1953 ), the eggs in this group move from the ovary to
the embryo sac through its wall by diapedesis and larvae
obviously escape through the body wall rupture. If so, the
function of the coelomopore may have shifted from egg to
statoblast release. Terminal tentacle pores are known in
Phylactolaemata (Hyatt 1866–1868 ; Nitsche 1868 ; Braem
1890 ; Marcus 1934 ), although sperm release via these pores
has yet to be confi rmed (see also Lützen et al. 2009 ).
There is no information concerning the presence of a SNP
in the Cyclostomata (Stenolaemata). Spawning is absent
since their larvae develop intracoelomically, later escaping
via the ooeciopore (gonozooidal orifi ce). The route for the
sperm is not known, but is presumed to be via a SNP. Since
tentacle pores are obviously not involved in sperm entry,
other theoretical options are (1) penetration of the tentacle
wall or even (2) ingestion.
It has been suggested that both Stenolaemata (Cyclostomata)
and Phylactolaemata possess derived patterns of sexual
reproduction (Ostrovsky et al. 2009a ). Both of these taxa have
small oligolecithal or mesolecithal eggs (Reed 1991 ) that
could have been spawned via the female gonopore in their
ancestor(s). Later in evolution, a shift in the reproductive
pattern involving viviparity (cyclostomes) and brooding
(phylactolaemates) could have led to loss of the primary
function (egg release) of the female gonopore. In both groups
the egg does not leave the maternal coelom; in Cyclostomata
an egg starts cleavage in the ovary, whereas in Phylactolaemata
the egg moves to the brood sac (i.e. outside the coelom)
without being released (Brien 1953 ; Reed 1991 ). The female
gonopore (SNP) is, however, supposedly used for sperm entry.
Theoretically, the existing SNP could have been either a
female gonopore or a nephridiopore in origin. In the
Phoronida, which were traditionally (but not invariably) considered as a related or even ancestral group for bryozoans
(Hyman 1959 ; Farmer et al. 1973 ; Farmer 1977 ; Ruppert
et al. 2004 ; but see Emig 1982 ; Nielsen 2001 ), sexual products are released via the paired nephridiopores of metanephridia. Similar to the bryozoan SNP, these pores are
positioned dorso-medially between the lophophore arms,
near the anus (Emig 1982 ; Zimmer 1991 ; Mukai et al. 1997 ).
It should be noted that both the phoronid and the phylactolaemate pore(s) under discussion lead to the main coelom
(metacoel), whereas in Gymnolaemata the female gonopore
leads to the lophophoral coelom that, in turn, is connected to
the main coelom (Hyman 1959 ; Mukai et al. 1997 ).
Although most molecular analyses do not support a close
relationships between Bryozoa and Phoronida (see
Introduction), the similarity in the position of pore(s) for
gamete release is obvious. Thus, it was suggested that an
ancestor of Bryozoa could have had a pore(s) similar to that
of phoronids, through which female gametes passed from the
visceral coelom to sea water and which also served for the
entry of allosperm (Ostrovsky and Porter 2011 ). The ciliated
internal structure associated with the pore, reminiscent of
phoronid metanephridia, would have been used to direct the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
ctenostome Zoobotryon verticillatum , but Silén did not
mention this fi nding. It should be stressed that, despite Silen’s
assumption, there is no evidence to date that the terminal
pores of tentacles were ever used by bryozoans as a conduit
for the entry of sperm. In some phoronids, however, the sperm
lyses through tentacle walls (Zimmer 1991 ).
Twenty years later it was discovered by Silén himself that
tentacles are male gonoducts in Bryozoa (Silén 1966 , 1972 ; see
also Bullivant 1967 ; Temkin 1994 ). In general, Silén’s speculations concerning the evolution of brooding, oviposition and
larval types in Gymnolaemata are highly disputable (criticized by Santagata and Banta 1996 and Ostrovsky 2009 ),
and were often based on wrongly interpreted facts. For instance,
his suggestion concerning the formation of the abovementioned “embryonary” (and thus speculations about egg release)
in ctenostomes is wrong since eggs immerse in the body wall
after their release (reviewed in Ström 1977 , see also Sect. 3.1.1 ).
According to the second hypothesis, the earliest Bryozoa
had a female gonopore (SNP) originally used both for spawning and for the entry of alien sperm, whereas terminal (coelomo)pores of the tentacles served as male gonopores for sperm
release. The ITO evolved later as an extension of the female
gonopore, retaining its functions (Ostrovsky and Porter 2011 ).
The difference between the two hypotheses on the origin
of the ITO is that in the fi rst case it supposedly evolved by
fusion of two entire dorso-medial tentacles, accompanied by
shortening and functional modifi cation (as a conduit for egg
release and sperm entry), while in the other, the ITO is
formed by the fusion of the basal parts of two dorso-medial
tentacles and did not change its function. In the fi rst case, the
terminal pore of the ITO corresponds to the male gonopore,
whereas in the second it is originated from the female one.
1.3.9.2 Origin of the Supraneural Coelomopore
Broadcasting is generally considered to be an ancestral
reproductive pattern in marine invertebrates (Jägersten 1972 ;
Levin and Bridges 1995 ; Havenhand 1995 ), including bryozoans (Zimmer and Woollacott 1977 ; Strathmann 1978 ;
Taylor 1988 ). In agreement with this idea, Reed ( 1991 ) stated
that the presence of an ITO is a primitive condition.
Ostrovsky and Porter ( 2011 ) agreed that the ITO evolved
early in the Bryozoa in broadcasting ctenostomes and cheilostomes. Nevertheless, they suggested that the initial state of
this character was a simple female gonopore that served for
both sperm entry and spawning in the earliest bryozoans. In
Phylactolaemata, a coelomopore in a vestibular wall through
which statoblasts, and, incidentally, sperm are released, has
been recorded by Marcus ( 1941a , 1942 ) and Wiebach ( 1953 ).
The position of this pore below the anus, at duplicature (i.e. at
the cystid wall) and not at the lophophore base, questions its
homology with the SNP in gymnolaemates (see also Marcus
1941a ). It may serve as a route for alien sperm. At the same
time, it is not known if it is used for oviposition. According
to Brien ( 1953 ), the eggs in this group move from the ovary to
the embryo sac through its wall by diapedesis and larvae
obviously escape through the body wall rupture. If so, the
function of the coelomopore may have shifted from egg to
statoblast release. Terminal tentacle pores are known in
Phylactolaemata (Hyatt 1866–1868 ; Nitsche 1868 ; Braem
1890 ; Marcus 1934 ), although sperm release via these pores
has yet to be confi rmed (see also Lützen et al. 2009 ).
There is no information concerning the presence of a SNP
in the Cyclostomata (Stenolaemata). Spawning is absent
since their larvae develop intracoelomically, later escaping
via the ooeciopore (gonozooidal orifi ce). The route for the
sperm is not known, but is presumed to be via a SNP. Since
tentacle pores are obviously not involved in sperm entry,
other theoretical options are (1) penetration of the tentacle
wall or even (2) ingestion.
It has been suggested that both Stenolaemata (Cyclostomata)
and Phylactolaemata possess derived patterns of sexual
reproduction (Ostrovsky et al. 2009a ). Both of these taxa have
small oligolecithal or mesolecithal eggs (Reed 1991 ) that
could have been spawned via the female gonopore in their
ancestor(s). Later in evolution, a shift in the reproductive
pattern involving viviparity (cyclostomes) and brooding
(phylactolaemates) could have led to loss of the primary
function (egg release) of the female gonopore. In both groups
the egg does not leave the maternal coelom; in Cyclostomata
an egg starts cleavage in the ovary, whereas in Phylactolaemata
the egg moves to the brood sac (i.e. outside the coelom)
without being released (Brien 1953 ; Reed 1991 ). The female
gonopore (SNP) is, however, supposedly used for sperm entry.
Theoretically, the existing SNP could have been either a
female gonopore or a nephridiopore in origin. In the
Phoronida, which were traditionally (but not invariably) considered as a related or even ancestral group for bryozoans
(Hyman 1959 ; Farmer et al. 1973 ; Farmer 1977 ; Ruppert
et al. 2004 ; but see Emig 1982 ; Nielsen 2001 ), sexual products are released via the paired nephridiopores of metanephridia. Similar to the bryozoan SNP, these pores are
positioned dorso-medially between the lophophore arms,
near the anus (Emig 1982 ; Zimmer 1991 ; Mukai et al. 1997 ).
It should be noted that both the phoronid and the phylactolaemate pore(s) under discussion lead to the main coelom
(metacoel), whereas in Gymnolaemata the female gonopore
leads to the lophophoral coelom that, in turn, is connected to
the main coelom (Hyman 1959 ; Mukai et al. 1997 ).
Although most molecular analyses do not support a close
relationships between Bryozoa and Phoronida (see
Introduction), the similarity in the position of pore(s) for
gamete release is obvious. Thus, it was suggested that an
ancestor of Bryozoa could have had a pore(s) similar to that
of phoronids, through which female gametes passed from the
visceral coelom to sea water and which also served for the
entry of allosperm (Ostrovsky and Porter 2011 ). The ciliated
internal structure associated with the pore, reminiscent of
phoronid metanephridia, would have been used to direct the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis