159
( Euginoma , Didymozoum , Anoteropora , hippothoomorphs,
Celleporidae, etc.) or only the kenozooidal ooecium is
present ( Cauloramphus ) (Ostrovsky et al. 2007 ).
Notwithstanding, why is the distal (auto)zooid reduced
and terminal ovicells formed? According to Bishop and
Househam ( 1987 ), the transformation of one type of ooecium into another is not an overly complex evolutionary step.
Judging from the fact that two categories of ooecia may be
present in one and the same colony, this supposition is likely
to be true. Nevertheless, the reasons for the reduction of the
distal zooid remain obscure.
The developing ooecium-producing distal zooid bud is
structurally identical to a kenozooid with an ooecium (compare Figs. 2.6a (B) and 2.18F ). The origin of this type of ooecium (type 1, category В) may be associated with the cessation
of distal autozooidal development after ooecium formation.
Why development ceases is, however, unclear. Harmelin and
Arístegui ( 1988 ) suggested that the formation of terminal ovicells of category С (sensu Bishop and Househam 1987 ) may
be indicative of an r-strategy. Conversely, ovicells that are a
product of two autozooids (category A) indicate a K-strategy.
In other words, they concluded that, whereas terminal ovicells (fi rst variant) ensure rapid formation of ooecia (and
early brooding), normal ovicells (second variant) are formed
less quickly but provide better protection for the embryo.
In many instances ooecia formed by the distal kenozooid
develop only at the colony periphery (in some Calloporidae
and Cribrilinidae) or on terminal areas of branches (in some
Calloporidae, Flustridae and Catenicellidae). For example,
terminal kenozooid-produced ovicells can be found at the
colony periphery in Callopora while autozooid-produced
ovicells occur at some distance from the periphery. It appears
that further budding of distal autozooids at the colony periphery is suppressed at the end of the growth period of the whole
colony, and because of that ooecia are formed by the distal
kenozooids there. This means that, at least in some cases,
terminal ovicells may result from age-related and/or astogenetic changes. On the other hand, in hippothoomorphs,
Celleporidae and Crepidacanthidae, the formation of terminal
ovicells does not depend on cessation of colony growth,
since these are the only kind of ovicells in the colony
(Ostrovsky et al. 2009a ). Corresponding examples among
cribrilinids are Cribrilina annulata and C . watersi and,
among chaperiids, Chaperiopsis cervicornis .
Insofar as all hippothoomorphs and the families
Celleporidae and Crepidacanthidae have terminal ovicells,
they probably inherited this character from their ancestors.
If so, the taxa of special interest would be those in which this
trend is best represented. Unsurprisingly, these are the most
ancient lineages of brooding cheilostomes – Calloporidae,
Microporidae and cribrimorphs. Three categories of ooecia
are found among them as well as in the stratigraphically
younger Bugulidae and Catenicellidae. This is unambiguous
evidence that terminal ovicells evolved independently in
different cheilostome clades by reduction of the ooeciumproducing zooid.
To return to the earlier question concerning the reason for
reduction of the distal zooid in cases when growth processes
are not an explanation – it may be conjectured that the evolution of terminal ovicells, which culminated in kenozooidal
ooecia (as in Cribrilina annulata and Cauloramphus ), was
associated with immersion of the brood cavity into the
colony (between zooids), which afforded better protection.
Comparative morphology shows that the brood cavity of
terminal ovicells is situated further below the colony surface
than that of hyperstomial ovicells formed by the distal autozooid (compare Figs. 2.6a (A, B, D, E) and b (A, B). Thus,
reduction of the distal zooid resulted in both immersion of
the brood cavity and in a transition from prominent to terminal
ovicells (corresponding to endozooidal and immersed
ovicells as regards the position of the brood cavity).
In the earliest stage of this transition, the distal autozooid was substituted by the distal kenozooid. Its degree of
reduction in different species varies, and terminal ovicells
are not always formed. Further reduction of the distal zooid
resulted in kenozooidal ooecia in some taxa, with the
brood cavity situated inside the maternal zooid
(Figs. 2.6b (A, B) and 2.29 ). In some cases the ooecium
was reduced to a vestigial kenozooidal ooecium, as in
Cauloramphus (Figs. 2.6b (E) and 2.25B ; see also Ostrovsky
et al. 2007 ) and some Beaniidae (Fig. 1.22 ). In some species the kenozooidal ooecium may still bud distal zooids
(Fig. 2.6b (B); see also Ostrovsky 1998 ), while in others
distal budding proceeds from the basal pore chambers of
the maternal zooid (Fig . 2.6b (C, E)).
The proportion of umbonulomorph and lepraliomorph
families and genera among bryozoans with terminal ovicells
is on the whole strikingly low. One family that does not conform to this rule is Celleporidae; all studied species have
ooecia formed by the distal kenozooid without distally distinct frontal part (Figs. 2.6b (F) and 2.42 ).
2.4.8.4 Immersion of the Brood Cavity
and Reduction of the Ooecium
As noted above, many brooding cheilostomes are characterized by immersion of the incubation cavity in the maternal or
distal zooid or in the colony (between zooids). This immersion, presumably ensuring better protection of the developing embryo, may be implemented in several ways. Apart
from terminal ovicells, it may be achieved by the formation
of a more concave ovicell fl oor, formed by the distal zooid,
representing the gradual transition from hyperstomial to
subimmersed to endozooidal (see Viskova 1992 ) or endotoichal ovicells. A third possibility involves invagination of the
distal wall of the maternal zooid, accompanied by reduction
of the calcifi ed brood-cavity fl oor and thus the transition to
2.4 Evolution of Brood Chambers in Cheilostomata
( Euginoma , Didymozoum , Anoteropora , hippothoomorphs,
Celleporidae, etc.) or only the kenozooidal ooecium is
present ( Cauloramphus ) (Ostrovsky et al. 2007 ).
Notwithstanding, why is the distal (auto)zooid reduced
and terminal ovicells formed? According to Bishop and
Househam ( 1987 ), the transformation of one type of ooecium into another is not an overly complex evolutionary step.
Judging from the fact that two categories of ooecia may be
present in one and the same colony, this supposition is likely
to be true. Nevertheless, the reasons for the reduction of the
distal zooid remain obscure.
The developing ooecium-producing distal zooid bud is
structurally identical to a kenozooid with an ooecium (compare Figs. 2.6a (B) and 2.18F ). The origin of this type of ooecium (type 1, category В) may be associated with the cessation
of distal autozooidal development after ooecium formation.
Why development ceases is, however, unclear. Harmelin and
Arístegui ( 1988 ) suggested that the formation of terminal ovicells of category С (sensu Bishop and Househam 1987 ) may
be indicative of an r-strategy. Conversely, ovicells that are a
product of two autozooids (category A) indicate a K-strategy.
In other words, they concluded that, whereas terminal ovicells (fi rst variant) ensure rapid formation of ooecia (and
early brooding), normal ovicells (second variant) are formed
less quickly but provide better protection for the embryo.
In many instances ooecia formed by the distal kenozooid
develop only at the colony periphery (in some Calloporidae
and Cribrilinidae) or on terminal areas of branches (in some
Calloporidae, Flustridae and Catenicellidae). For example,
terminal kenozooid-produced ovicells can be found at the
colony periphery in Callopora while autozooid-produced
ovicells occur at some distance from the periphery. It appears
that further budding of distal autozooids at the colony periphery is suppressed at the end of the growth period of the whole
colony, and because of that ooecia are formed by the distal
kenozooids there. This means that, at least in some cases,
terminal ovicells may result from age-related and/or astogenetic changes. On the other hand, in hippothoomorphs,
Celleporidae and Crepidacanthidae, the formation of terminal
ovicells does not depend on cessation of colony growth,
since these are the only kind of ovicells in the colony
(Ostrovsky et al. 2009a ). Corresponding examples among
cribrilinids are Cribrilina annulata and C . watersi and,
among chaperiids, Chaperiopsis cervicornis .
Insofar as all hippothoomorphs and the families
Celleporidae and Crepidacanthidae have terminal ovicells,
they probably inherited this character from their ancestors.
If so, the taxa of special interest would be those in which this
trend is best represented. Unsurprisingly, these are the most
ancient lineages of brooding cheilostomes – Calloporidae,
Microporidae and cribrimorphs. Three categories of ooecia
are found among them as well as in the stratigraphically
younger Bugulidae and Catenicellidae. This is unambiguous
evidence that terminal ovicells evolved independently in
different cheilostome clades by reduction of the ooeciumproducing zooid.
To return to the earlier question concerning the reason for
reduction of the distal zooid in cases when growth processes
are not an explanation – it may be conjectured that the evolution of terminal ovicells, which culminated in kenozooidal
ooecia (as in Cribrilina annulata and Cauloramphus ), was
associated with immersion of the brood cavity into the
colony (between zooids), which afforded better protection.
Comparative morphology shows that the brood cavity of
terminal ovicells is situated further below the colony surface
than that of hyperstomial ovicells formed by the distal autozooid (compare Figs. 2.6a (A, B, D, E) and b (A, B). Thus,
reduction of the distal zooid resulted in both immersion of
the brood cavity and in a transition from prominent to terminal
ovicells (corresponding to endozooidal and immersed
ovicells as regards the position of the brood cavity).
In the earliest stage of this transition, the distal autozooid was substituted by the distal kenozooid. Its degree of
reduction in different species varies, and terminal ovicells
are not always formed. Further reduction of the distal zooid
resulted in kenozooidal ooecia in some taxa, with the
brood cavity situated inside the maternal zooid
(Figs. 2.6b (A, B) and 2.29 ). In some cases the ooecium
was reduced to a vestigial kenozooidal ooecium, as in
Cauloramphus (Figs. 2.6b (E) and 2.25B ; see also Ostrovsky
et al. 2007 ) and some Beaniidae (Fig. 1.22 ). In some species the kenozooidal ooecium may still bud distal zooids
(Fig. 2.6b (B); see also Ostrovsky 1998 ), while in others
distal budding proceeds from the basal pore chambers of
the maternal zooid (Fig . 2.6b (C, E)).
The proportion of umbonulomorph and lepraliomorph
families and genera among bryozoans with terminal ovicells
is on the whole strikingly low. One family that does not conform to this rule is Celleporidae; all studied species have
ooecia formed by the distal kenozooid without distally distinct frontal part (Figs. 2.6b (F) and 2.42 ).
2.4.8.4 Immersion of the Brood Cavity
and Reduction of the Ooecium
As noted above, many brooding cheilostomes are characterized by immersion of the incubation cavity in the maternal or
distal zooid or in the colony (between zooids). This immersion, presumably ensuring better protection of the developing embryo, may be implemented in several ways. Apart
from terminal ovicells, it may be achieved by the formation
of a more concave ovicell fl oor, formed by the distal zooid,
representing the gradual transition from hyperstomial to
subimmersed to endozooidal (see Viskova 1992 ) or endotoichal ovicells. A third possibility involves invagination of the
distal wall of the maternal zooid, accompanied by reduction
of the calcifi ed brood-cavity fl oor and thus the transition to
2.4 Evolution of Brood Chambers in Cheilostomata