66
The evolution of sexual polymorphism is a striking example
of how colonial integration is progressively enhanced
through specialization of their cystid and/or polypide
modules, some of which may be arranged to function as
colonial “organs.” Such colonial integration is expressed in
the formation of morpho-functional modules of maternal and
ooecium- forming zooids (see Sect. 2.4.8 ).
The so-called “dwarf” or “dimorphic-female” zooids of
Cribrilina annulata (Cribrilinidae) (see Powell 1967a ) are hermaphrodite autozooids. They are smaller than other zooids and
their cystid partly lies on the frontal surface of the colony. They
bud, as do all other zooids, from distal or distolateral pore
chambers (and not from some “frontal dietellae” as suggested
by Powell, who made no sections), growing not along the substratum but upwards. It has been suggested that lack of suffi -
cient space for the formation of a normal zooid may result in
vertical growth of the proximal part of the bud while its distal
part will be formed at the colony surface (Ostrovsky 1998 ).
It should be noted that, in some cases, zooids may
change sex or acquire it. This phenomenon was observed in
overwintered colonies of Chartella papyracea , in which
many of the former female zooids that lost their ovary in
autumn developed spermatogenic tissue in spring (Dyrynda
and Ryland 1982 ). In Celleporella hyalina , Antarctothoa
bougainvillei and A . tongima , some autozooids may become
males after 1–2 months of normal functioning (Cancino
and Hughes 1988 ; Rogick 1956 ; Powell 1967b ). In the latter species some female zooids may become male, the
acquisition/change of sex being accompanied by intramural
budding, resulting in the formation of a dwarf male cystid
inside the initial one (Powell 1967b ), and male cystids may
also be initiated following a check in colony growth
(Gordon 1968b ). Zooids may likewise acquire sex through
reparative budding following mechanical damage. For
instance, I found a single reparative male zooid formed
inside a former autozooidal cystid in Antarctothoa sp.
1.3.9 Evolution of Intertentacular Organ
In Bryozoa, ripe gametes leave the coelomic cavity via (1)
terminal tentacle pores (male gonopores) or (2) the female
gonopore, represented either by a supraneural coelomopore
(SNP) or a terminal opening of the intertentacular organ
(ITO) (Calvet 1900 ; Marcus 1926a , b ; Cori 1941 ; Hyman
1959 ; Brien 1960 ; Silén 1966 ; Reed 1991 ; Temkin 1994 ;
Mukai et al. 1997 ; Woollacott 1999 ). The coelomopore and
intertentacular organ occupy the same position at the base of
the tentacle crown, close to the ganglion and between the
bases of the two dorso-medial tentacles. Silén ( 1945 ) considered the ITO and coelomopore as homologous structures as
they have the same position and function. Later, Reed ( 1991 ,
p. 140) called the ITO an extension of the female gonopore.
The ITO is known only in gymnolaemates (Fig. 1.1C ). It is
a two-chambered tube, ranging from about one quarter to one
third of the tentacle length. The proximal chamber has a
glandular structure (Temkin 1994 ). The distal pore is directed
away from the funnel of the lophophore. The ITO is heavily
ciliated internally (see Prouho 1892 , pl. 16, fi gs. 47–48, 52
and 56; Calvet 1900 , pl. 6, fi gs. 8 and 10, pl. 7, fi g. 11; Silén
1966 , fi g. 15). In the broadcasting cheilostome Membranipora
serrilamella , it is connected with an internal ciliated gutter
(Hageman 1981 ; Reed 1991 ). Similar internal ciliated
structures have been recorded in the brooding ctenostomes
Alcyonidium polyoum and Bowerbankia gracilis (Matricon
1963 ; Reed 1988 ). Both species have a SNP, which is associated
with the internal ciliated funnel in A. polyoum and with a pair
of longitudinal ciliated ridges (also internal) in B . gracilis .
Reed ( 1991 ) suggested that these structures (ciliated gutter,
funnel and longitudinal ridges) are homologous.
In M . serrilamella , the ITO develops at the onset of oogenesis, and the whole process lasts about 2 days. The outer epithelium differentiates from rows of abfrontal and fronto-lateral
cells of the two dorso-medial tentacles. The internal cells of
the ITO differentiate from lateral cells of the tentacles, which
lose their cilia and later develop new ciliation (Hageman
1981 ). The differentiation of the ITO is not connected with
polypide replacement (Cori 1941 ; Jebram 1975 ; Reed 1991 ;
see also Cook 1962 ; Silén 1966 ; Jebram 1973 ; Cadman and
Ryland 1996 ). It is not yet known if the SNP is present before
the formation of the ITO or if it occurs in non-fertile zooids.
The supraneural coelomopore (SNP) (the term was introduced by Marcus 1926a , 1938a ) is very small, and was fi rst
encountered during observation of egg spawning in the
ctenostome Farrella repens by van Beneden ( 1844a ) (see
also Prouho 1892 ; Marcus 1926a , b , 1938a ; Cori 1941 ; Silén
1945 ; Ostrovsky et al. 2008 ). The ITO was initially discovered in the ctenostome Alcyonidium duplex by Farre ( 1837 ,
p. 408) who wondered whether “it indicate[s] a difference
of sex?” The ITO, apparently releasing sperm, was later
observed in the cheilostome Electra pilosa by Hincks ( 1851 ),
who introduced the term “intertentacular organ” (see also
Hincks 1880 ). Ehlers ( 1876 ) observed the presence of an
ITO in almost all zooids of an unidentifi ed cheilostome.
Although Ehlers referred to the earlier work (Farre 1837 ;
Hincks 1851 ), he suggested that the ITO was an attached
parasitic infusorian. Later, Hincks ( 1880 ) and Harmer ( 1892 )
ascribed an excretory function to this organ.
The ITO was later shown to be similar in function to the
SNP, serving as a route for the release of eggs in a variety of
species (Prouho 1889 , 1892 ; Schulz 1901 ; Marcus 1926a , b ;
Eggleston 1963 ; Silén 1966 ; Mawatari 1975 ; Jebram 1975 ;
Temkin 1994 ; Ryland 2001 ; Temkin and Bortolami 2004 ).
The ITO also serves as the entry point for sperm (Temkin
1994 ). This function has also been ascribed (but not documented) to the SNP. Hincks ( 1880 ) and Prouho ( 1892 )
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
The evolution of sexual polymorphism is a striking example
of how colonial integration is progressively enhanced
through specialization of their cystid and/or polypide
modules, some of which may be arranged to function as
colonial “organs.” Such colonial integration is expressed in
the formation of morpho-functional modules of maternal and
ooecium- forming zooids (see Sect. 2.4.8 ).
The so-called “dwarf” or “dimorphic-female” zooids of
Cribrilina annulata (Cribrilinidae) (see Powell 1967a ) are hermaphrodite autozooids. They are smaller than other zooids and
their cystid partly lies on the frontal surface of the colony. They
bud, as do all other zooids, from distal or distolateral pore
chambers (and not from some “frontal dietellae” as suggested
by Powell, who made no sections), growing not along the substratum but upwards. It has been suggested that lack of suffi -
cient space for the formation of a normal zooid may result in
vertical growth of the proximal part of the bud while its distal
part will be formed at the colony surface (Ostrovsky 1998 ).
It should be noted that, in some cases, zooids may
change sex or acquire it. This phenomenon was observed in
overwintered colonies of Chartella papyracea , in which
many of the former female zooids that lost their ovary in
autumn developed spermatogenic tissue in spring (Dyrynda
and Ryland 1982 ). In Celleporella hyalina , Antarctothoa
bougainvillei and A . tongima , some autozooids may become
males after 1–2 months of normal functioning (Cancino
and Hughes 1988 ; Rogick 1956 ; Powell 1967b ). In the latter species some female zooids may become male, the
acquisition/change of sex being accompanied by intramural
budding, resulting in the formation of a dwarf male cystid
inside the initial one (Powell 1967b ), and male cystids may
also be initiated following a check in colony growth
(Gordon 1968b ). Zooids may likewise acquire sex through
reparative budding following mechanical damage. For
instance, I found a single reparative male zooid formed
inside a former autozooidal cystid in Antarctothoa sp.
1.3.9 Evolution of Intertentacular Organ
In Bryozoa, ripe gametes leave the coelomic cavity via (1)
terminal tentacle pores (male gonopores) or (2) the female
gonopore, represented either by a supraneural coelomopore
(SNP) or a terminal opening of the intertentacular organ
(ITO) (Calvet 1900 ; Marcus 1926a , b ; Cori 1941 ; Hyman
1959 ; Brien 1960 ; Silén 1966 ; Reed 1991 ; Temkin 1994 ;
Mukai et al. 1997 ; Woollacott 1999 ). The coelomopore and
intertentacular organ occupy the same position at the base of
the tentacle crown, close to the ganglion and between the
bases of the two dorso-medial tentacles. Silén ( 1945 ) considered the ITO and coelomopore as homologous structures as
they have the same position and function. Later, Reed ( 1991 ,
p. 140) called the ITO an extension of the female gonopore.
The ITO is known only in gymnolaemates (Fig. 1.1C ). It is
a two-chambered tube, ranging from about one quarter to one
third of the tentacle length. The proximal chamber has a
glandular structure (Temkin 1994 ). The distal pore is directed
away from the funnel of the lophophore. The ITO is heavily
ciliated internally (see Prouho 1892 , pl. 16, fi gs. 47–48, 52
and 56; Calvet 1900 , pl. 6, fi gs. 8 and 10, pl. 7, fi g. 11; Silén
1966 , fi g. 15). In the broadcasting cheilostome Membranipora
serrilamella , it is connected with an internal ciliated gutter
(Hageman 1981 ; Reed 1991 ). Similar internal ciliated
structures have been recorded in the brooding ctenostomes
Alcyonidium polyoum and Bowerbankia gracilis (Matricon
1963 ; Reed 1988 ). Both species have a SNP, which is associated
with the internal ciliated funnel in A. polyoum and with a pair
of longitudinal ciliated ridges (also internal) in B . gracilis .
Reed ( 1991 ) suggested that these structures (ciliated gutter,
funnel and longitudinal ridges) are homologous.
In M . serrilamella , the ITO develops at the onset of oogenesis, and the whole process lasts about 2 days. The outer epithelium differentiates from rows of abfrontal and fronto-lateral
cells of the two dorso-medial tentacles. The internal cells of
the ITO differentiate from lateral cells of the tentacles, which
lose their cilia and later develop new ciliation (Hageman
1981 ). The differentiation of the ITO is not connected with
polypide replacement (Cori 1941 ; Jebram 1975 ; Reed 1991 ;
see also Cook 1962 ; Silén 1966 ; Jebram 1973 ; Cadman and
Ryland 1996 ). It is not yet known if the SNP is present before
the formation of the ITO or if it occurs in non-fertile zooids.
The supraneural coelomopore (SNP) (the term was introduced by Marcus 1926a , 1938a ) is very small, and was fi rst
encountered during observation of egg spawning in the
ctenostome Farrella repens by van Beneden ( 1844a ) (see
also Prouho 1892 ; Marcus 1926a , b , 1938a ; Cori 1941 ; Silén
1945 ; Ostrovsky et al. 2008 ). The ITO was initially discovered in the ctenostome Alcyonidium duplex by Farre ( 1837 ,
p. 408) who wondered whether “it indicate[s] a difference
of sex?” The ITO, apparently releasing sperm, was later
observed in the cheilostome Electra pilosa by Hincks ( 1851 ),
who introduced the term “intertentacular organ” (see also
Hincks 1880 ). Ehlers ( 1876 ) observed the presence of an
ITO in almost all zooids of an unidentifi ed cheilostome.
Although Ehlers referred to the earlier work (Farre 1837 ;
Hincks 1851 ), he suggested that the ITO was an attached
parasitic infusorian. Later, Hincks ( 1880 ) and Harmer ( 1892 )
ascribed an excretory function to this organ.
The ITO was later shown to be similar in function to the
SNP, serving as a route for the release of eggs in a variety of
species (Prouho 1889 , 1892 ; Schulz 1901 ; Marcus 1926a , b ;
Eggleston 1963 ; Silén 1966 ; Mawatari 1975 ; Jebram 1975 ;
Temkin 1994 ; Ryland 2001 ; Temkin and Bortolami 2004 ).
The ITO also serves as the entry point for sperm (Temkin
1994 ). This function has also been ascribed (but not documented) to the SNP. Hincks ( 1880 ) and Prouho ( 1892 )
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis