64
sexual reproduction” as gonozooids. He also divided them into
female (gynozooids) and male (androzooids), but this terminology has been used only rarely.
The term “gonozooid” is currently used for enlarged zooids
specialized for intracoelomic incubation of embryos in cyclostome bryozoans. The presumptive gonozooid notably has
a functional or rudimentary (but presumably protrusible)
polypide (reviewed in Reed 1991 ) thus being an autozooidal
polymorph, not a heterozooid as generally considered.
Hageman ( 1983 ) described four forms of “sexual dimorphism” in Bryozoa. Slightly modifi ed, this classifi cation is as
follows.
1. Species in which sexual zooids (gonochoristic male
and female zooids and hermaphrodites) are morphologically
the same as sterile autozooids. This is the commonest form
of sexual polymorphism, examples of which have been
described above.
2. Species in which cystid morphology in gonochoristic
female or hermaphrodite zooids differs from that of sterile
autozooids through enlargement or reduction, sometimes
accompanied by changes in shape (e.g. Fig. 1.36A, B ).
For example, enlargement of zooids and zooid openings
in such internal brooders as Adeonidae and Reciprocus regalis (Urceoliporidae) is associated with brooding of the large
larvae that develop in the internal brood sac (Waters 1912 ,
1913 ; Cook 1973 ; my data). Whereas brooding zooids
in Adeonella calveti are gonochoristic females, those in
R. regalis are hermaphrodite. These cheilostomes are matrotrophic, and it is rather obvious that zooid enlargement is a
consequence of embryo enlargement. Thus, matrotrophy
may have triggered sexual polymorphism in at least some
clades or species (Ostrovsky 2013 ) (see also Sect. 3.3 ). Also,
female zooids are the largest in colonies of viviparous,
matrotrophic Epistomia (Dyrynda 1981 ; Dyrynda and King
1982 ; Winston 2004 ). In the epistomiid Synnotum sp. the
size difference is not so obvious although the female zooids
are slightly swollen compared to the others (Marcus 1941b ).
EEN may equally have resulted in the evolution of polyembryony and enlarged gonozooids in the Stenolaemata.
In this regard, it should be noted that zooidal polymorphs
can sometimes occupy a strictly defi ned position in the
colony. For example, in Chlidonia pyriformis (Chlidoniidae),
the larger brooding (female) autozooids are always formed
fi rst (and are thus basal) in every branch containing such
zooids (see also Silén 1977 ). Although based on very limited
material, this species seems non-matrotrophic, and, thus, the
enlargement of the brooding zooids is obviously connected
with large oocyte size. It is not known if incubation is matrotropic in Bryopastoridae. In the internally brooding species
of this family, female zooids differ from regular autozooids
in having a larger opesia and thus a more voluminous internal
cavity. Morever the distal part of the female polymorph is
broader and longer (spoon-like), whereas the upper edge of
the distal wall rises slightly above the colony surface (see
also Gordon 1986 ). Also, the fertile zooids in the internal
brooder Pleurotoichus clathratus (Euthyrisellidae) have a
broader opercular base. At the proximal edge of the more
distal zooids a soft spine is formed.
When the embryo is brooded in the ovicell, differences
usually concern only the opening of the fertile zooid.
In Micropora notialis (Microporidae), Pacifi cincola insculpta
(Pacifi cincolidae), “Calyptotheca” variolosa (Lanceoporidae)
and Myriapora truncata (Myriaporidae), the openings of
fertile autozooids are somewhat larger than those of other
autozooids and have a different shape (see also Nielsen
1981 ). The frontal skeletal wall of the fertile autozooid in
Selenariopsis gabrieli (Eurystomellidae) is shorter than that
of the autozooid (Fig. 2.7a (H)) and its operculum is elongated
not longitudinally but transversally. Fertile zooids in confamilial Eurystomella species are typically slightly broader
than other autozooids and have a correspondingly larger operculum (see also Gordon 1984 ). The same is true of the species
of Lanceoporidae (see also Reverter-Gil et al. 2012 ). Further,
as can be seen in sections, female opercula may be much
thicker than regular opercula (e.g. Emballotheca quadrata ,
Lanceoporidae).
In Quadriscutella papillata (Phorioppniidae), female
polymorphs are much larger than other zooids, differing
from them also in the shape of the cystid and the operculum
and the size and number of pseudopores in the frontal shield.
Fertile catenicellid zooids have larger cystids and opercula
than sterile zooids, often accompanied by differences in
pseudopores, adventitious avicularia and other features.
Among Catenicellidae the female zooid develops as part of a
complex that includes the brood chamber (ovicell) and a distal zooid ( Pterocella scutella ) or it has only a terminal ovicell
( Costaticella ). Wass and Banta ( 1981 ) referred to these structures as “ovicell complexes” (see Figs. 1.25A and 2.6a (D)).
Fertile zooids in Cornucopina polymorpha (Bugulidae)
slightly differ from sterile ones in cystid size and shape, the
latter being longer and narrower. Moreover, in sterile autozooids the distal part is elongated, whereas in fertile ones it
is abruptly slanted and rounded.
(3) The next category includes species in which sexual
polymorphs differ from sterile zooids only (or primarily) in
polypide morphology. For example, Silén ( 1977 ) considered
formation of lophophores with an intertentacular organ as a
manifestation of seasonal sexual dimorphism (mostly concerning malacostegans). Female polypides in Thalamoporella
evelinae and T. californica (Thalamoporellidae) have only
14 tentacles, while male and sterile ones have 17 (Marcus
1941a ; Hastings 1930 ). The polymorphs are also smaller and
their functions apparently differ. Hastings ( 1930 ) thought
that the only function of small female polypides in T. californica is oviposition, since their short tentacles, owing to the
position of the ovicell, may reach only into the cavity of the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
sexual reproduction” as gonozooids. He also divided them into
female (gynozooids) and male (androzooids), but this terminology has been used only rarely.
The term “gonozooid” is currently used for enlarged zooids
specialized for intracoelomic incubation of embryos in cyclostome bryozoans. The presumptive gonozooid notably has
a functional or rudimentary (but presumably protrusible)
polypide (reviewed in Reed 1991 ) thus being an autozooidal
polymorph, not a heterozooid as generally considered.
Hageman ( 1983 ) described four forms of “sexual dimorphism” in Bryozoa. Slightly modifi ed, this classifi cation is as
follows.
1. Species in which sexual zooids (gonochoristic male
and female zooids and hermaphrodites) are morphologically
the same as sterile autozooids. This is the commonest form
of sexual polymorphism, examples of which have been
described above.
2. Species in which cystid morphology in gonochoristic
female or hermaphrodite zooids differs from that of sterile
autozooids through enlargement or reduction, sometimes
accompanied by changes in shape (e.g. Fig. 1.36A, B ).
For example, enlargement of zooids and zooid openings
in such internal brooders as Adeonidae and Reciprocus regalis (Urceoliporidae) is associated with brooding of the large
larvae that develop in the internal brood sac (Waters 1912 ,
1913 ; Cook 1973 ; my data). Whereas brooding zooids
in Adeonella calveti are gonochoristic females, those in
R. regalis are hermaphrodite. These cheilostomes are matrotrophic, and it is rather obvious that zooid enlargement is a
consequence of embryo enlargement. Thus, matrotrophy
may have triggered sexual polymorphism in at least some
clades or species (Ostrovsky 2013 ) (see also Sect. 3.3 ). Also,
female zooids are the largest in colonies of viviparous,
matrotrophic Epistomia (Dyrynda 1981 ; Dyrynda and King
1982 ; Winston 2004 ). In the epistomiid Synnotum sp. the
size difference is not so obvious although the female zooids
are slightly swollen compared to the others (Marcus 1941b ).
EEN may equally have resulted in the evolution of polyembryony and enlarged gonozooids in the Stenolaemata.
In this regard, it should be noted that zooidal polymorphs
can sometimes occupy a strictly defi ned position in the
colony. For example, in Chlidonia pyriformis (Chlidoniidae),
the larger brooding (female) autozooids are always formed
fi rst (and are thus basal) in every branch containing such
zooids (see also Silén 1977 ). Although based on very limited
material, this species seems non-matrotrophic, and, thus, the
enlargement of the brooding zooids is obviously connected
with large oocyte size. It is not known if incubation is matrotropic in Bryopastoridae. In the internally brooding species
of this family, female zooids differ from regular autozooids
in having a larger opesia and thus a more voluminous internal
cavity. Morever the distal part of the female polymorph is
broader and longer (spoon-like), whereas the upper edge of
the distal wall rises slightly above the colony surface (see
also Gordon 1986 ). Also, the fertile zooids in the internal
brooder Pleurotoichus clathratus (Euthyrisellidae) have a
broader opercular base. At the proximal edge of the more
distal zooids a soft spine is formed.
When the embryo is brooded in the ovicell, differences
usually concern only the opening of the fertile zooid.
In Micropora notialis (Microporidae), Pacifi cincola insculpta
(Pacifi cincolidae), “Calyptotheca” variolosa (Lanceoporidae)
and Myriapora truncata (Myriaporidae), the openings of
fertile autozooids are somewhat larger than those of other
autozooids and have a different shape (see also Nielsen
1981 ). The frontal skeletal wall of the fertile autozooid in
Selenariopsis gabrieli (Eurystomellidae) is shorter than that
of the autozooid (Fig. 2.7a (H)) and its operculum is elongated
not longitudinally but transversally. Fertile zooids in confamilial Eurystomella species are typically slightly broader
than other autozooids and have a correspondingly larger operculum (see also Gordon 1984 ). The same is true of the species
of Lanceoporidae (see also Reverter-Gil et al. 2012 ). Further,
as can be seen in sections, female opercula may be much
thicker than regular opercula (e.g. Emballotheca quadrata ,
Lanceoporidae).
In Quadriscutella papillata (Phorioppniidae), female
polymorphs are much larger than other zooids, differing
from them also in the shape of the cystid and the operculum
and the size and number of pseudopores in the frontal shield.
Fertile catenicellid zooids have larger cystids and opercula
than sterile zooids, often accompanied by differences in
pseudopores, adventitious avicularia and other features.
Among Catenicellidae the female zooid develops as part of a
complex that includes the brood chamber (ovicell) and a distal zooid ( Pterocella scutella ) or it has only a terminal ovicell
( Costaticella ). Wass and Banta ( 1981 ) referred to these structures as “ovicell complexes” (see Figs. 1.25A and 2.6a (D)).
Fertile zooids in Cornucopina polymorpha (Bugulidae)
slightly differ from sterile ones in cystid size and shape, the
latter being longer and narrower. Moreover, in sterile autozooids the distal part is elongated, whereas in fertile ones it
is abruptly slanted and rounded.
(3) The next category includes species in which sexual
polymorphs differ from sterile zooids only (or primarily) in
polypide morphology. For example, Silén ( 1977 ) considered
formation of lophophores with an intertentacular organ as a
manifestation of seasonal sexual dimorphism (mostly concerning malacostegans). Female polypides in Thalamoporella
evelinae and T. californica (Thalamoporellidae) have only
14 tentacles, while male and sterile ones have 17 (Marcus
1941a ; Hastings 1930 ). The polymorphs are also smaller and
their functions apparently differ. Hastings ( 1930 ) thought
that the only function of small female polypides in T. californica is oviposition, since their short tentacles, owing to the
position of the ovicell, may reach only into the cavity of the
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis