124
cells (in strongly calcifi ed old ooecia), the absence of specialized pore-cell complexes does not allow one to consider
such ooecia as polymorphs (Ostrovsky and Schäfer 2003 ;
Ostrovsky et al. 2009a ). To sum up, in the majority of cheilostomes, ooecia are body-wall outgrowths, not heterozooids
(an alternative viewpoint is endorsed by Viskova 1992 ).
At the same time, ooecia evolved from spines (except in
Scruparia , Alysidium and Catenicula ; see Ostrovsky and
Taylor 2004 , 2005a ), which are obviously modifi ed modular
polymorphs (Silén 1942 ; see also Lidgard et al. 2012 ).
Ultrastructure and development of ovicells have been
studied in additional calloporids ( Callopora , Tegella ,
Corbulella ) (Ostrovsky et al. 2003 ). Taylor and MacKinney
( 2002 ) and Ostrovsky ( 2002 ) described the structure of
so- called “costate” ovicells in some fossil and Recent
Microporidae and Cribrilinidae, correspondingly, and discussed the origin of ovicells in cheilostomes. Ostrovsky and
Taylor ( 2004 ) described four calloporid species in which the
brood chambers were formed by spines of the daughter zooid
in Middle Cretaceous material from England and Germany.
Such primitive ovicells looked like a cage, on the one hand
supporting Harmer’s hypothesis ( 1902 ) that the ovicell
originated from mural spines, and on the other hand
according with Nielsen’s view ( 1985 ) that category A ovicells (ooecium formed by the distal autozooid) are basic in
ovicell evolution. A detailed survey of the fossil and Recent
cheilostomes whose brood chambers consist of spines or
costae has been published by Ostrovsky and Taylor ( 2005a ).
The development of the ooecium has additionally been
investigated in the earliest cheilostome brooders, belonging
to the genus Wilbertopora . Interestingly, it is different
from ovicellogenesis in Recent calloporids, being more
reminiscent of that in Recent cribrimorphs such as Puellina
(discussed in Ostrovsky and Taylor 2005b ).
More recently, research has been presented on the anatomy
of ovicells and internal brood sacs in a number of anascan
cheilostomes (Ostrovsky et al. 2006 , 2007 , 2009a , b ) as well
as two large reviews on brooding structures and the history of
research on cheilostome parental care (Ostrovsky 2008a , b ).
In the sections that follow, the main types of cheilostome brood chambers (both development and structure) are
described using correlated light-microscopic and SEM
techniques. An emended classifi cation and terminology are
proposed. Hypotheses on the origin of chambers for embryo
incubation are discussed together with the main trends in
their evolution.
2.2
Classifi cation and Terminology
Chambers for embryo incubation are among the most
important characters in the systematics of Bryozoa, particularly in the Cheilostomata (Viskova 1992 ; Ostrovsky 2004 ,
2008b ). However, a review of the literature shows that many
authors used the terms introduced by the early scholars
(Hincks 1880 ; Jullien 1888 ; Levinsen 1902 , 1909 ; Canu and
Bassler 1920 ) rather arbitrarily, and there is much inconsistency in older taxonomic descriptions. Many taxonomists
still rely on the terminology and schematic illustrations of
Bassler ( 1953 ), who applied the terms of Levinsen ( 1902 ,
1909 ) to the schematics of Canu and Bassler ( 1920 ) (see
above). Ryland ( 1968 , 1970 , 1976 , 1979 ) and Ryland and
Hayward ( 1977 ) simplifi ed and improved the terminology,
stressing the main principles upon which such terminology
should be based (see Ostrovsky 2008b ). However, cheilostome brood chambers are very diverse, and in the absence of
a clear understanding of their internal structure, the situation
has been far from satisfactory. The terminology of the earlier
authors that later became standard has carried with it the
baggage of over-simplifi ed, even erroneous, ideas about
brood-chamber structure (discussed in Ostrovsky 2008b ).
As a result, taxonomists have continued to use the terms that
they prefer, which are often in contradiction with the actual
structure of the brood chamber.
An extensive review of cheilostome brooding structures
was recently published, aiming to correct this situation
(Ostrovsky 2008b ). It featured descriptions of the range of
different morphologies and a revision of terminology
commonly used in taxonomic descriptions. The traditional
morpho- functional terminological approach has been supplemented by a developmental approach. In the following
section, a revised and expanded version of this review is
presented.
Four main groups of embryo-incubation chambers are
known in Cheilostomata: (1) external membranous sacs
( Aetea , Eucratea loricata , “ Carbasea ” indivisa , Leiosalpinx
australis ); (2) skeletal (calcifi ed) chambers, including all
ovicells and brood chambers formed by spines (most cheilostomes); (3) internal brood sacs formed by non-calcifi ed
zooidal walls (in at least 22 families); and (4) female zooids
for intracoelomic incubation (Epistomiidae). This division is
based on wall composition and positioning of the brood
chamber (Ostrovsky 2008a , b ).
We still do not know how the chamber wall is formed in
the fi rst group and of what it consists (Fig. 2.52 ). Various
authors have suggested it to be an outgrowth of the introvert
wall, a cuticular chamber produced by the external cystid
wall or a sticky fertilization envelope (Stach 1938 ; Cook
1977b ; Ström 1977 ). In any case, the term “external membranous brood sac” should be applied to them all. Notably,
all cheilostomes possessing these sacs have simple skeletal
morphology and are considered to be less derived.
The second group covers the majority of incubation
chambers known in Cheilostomata. Apart from the acanthostegal brood chambers of Tendridae (“acanthostegous
ooecia” of Levinsen 1902 , 1909 ), which are represented by
2 Cheilostome Brood Chambers: Structure, Formation, Evolution
cells (in strongly calcifi ed old ooecia), the absence of specialized pore-cell complexes does not allow one to consider
such ooecia as polymorphs (Ostrovsky and Schäfer 2003 ;
Ostrovsky et al. 2009a ). To sum up, in the majority of cheilostomes, ooecia are body-wall outgrowths, not heterozooids
(an alternative viewpoint is endorsed by Viskova 1992 ).
At the same time, ooecia evolved from spines (except in
Scruparia , Alysidium and Catenicula ; see Ostrovsky and
Taylor 2004 , 2005a ), which are obviously modifi ed modular
polymorphs (Silén 1942 ; see also Lidgard et al. 2012 ).
Ultrastructure and development of ovicells have been
studied in additional calloporids ( Callopora , Tegella ,
Corbulella ) (Ostrovsky et al. 2003 ). Taylor and MacKinney
( 2002 ) and Ostrovsky ( 2002 ) described the structure of
so- called “costate” ovicells in some fossil and Recent
Microporidae and Cribrilinidae, correspondingly, and discussed the origin of ovicells in cheilostomes. Ostrovsky and
Taylor ( 2004 ) described four calloporid species in which the
brood chambers were formed by spines of the daughter zooid
in Middle Cretaceous material from England and Germany.
Such primitive ovicells looked like a cage, on the one hand
supporting Harmer’s hypothesis ( 1902 ) that the ovicell
originated from mural spines, and on the other hand
according with Nielsen’s view ( 1985 ) that category A ovicells (ooecium formed by the distal autozooid) are basic in
ovicell evolution. A detailed survey of the fossil and Recent
cheilostomes whose brood chambers consist of spines or
costae has been published by Ostrovsky and Taylor ( 2005a ).
The development of the ooecium has additionally been
investigated in the earliest cheilostome brooders, belonging
to the genus Wilbertopora . Interestingly, it is different
from ovicellogenesis in Recent calloporids, being more
reminiscent of that in Recent cribrimorphs such as Puellina
(discussed in Ostrovsky and Taylor 2005b ).
More recently, research has been presented on the anatomy
of ovicells and internal brood sacs in a number of anascan
cheilostomes (Ostrovsky et al. 2006 , 2007 , 2009a , b ) as well
as two large reviews on brooding structures and the history of
research on cheilostome parental care (Ostrovsky 2008a , b ).
In the sections that follow, the main types of cheilostome brood chambers (both development and structure) are
described using correlated light-microscopic and SEM
techniques. An emended classifi cation and terminology are
proposed. Hypotheses on the origin of chambers for embryo
incubation are discussed together with the main trends in
their evolution.
2.2
Classifi cation and Terminology
Chambers for embryo incubation are among the most
important characters in the systematics of Bryozoa, particularly in the Cheilostomata (Viskova 1992 ; Ostrovsky 2004 ,
2008b ). However, a review of the literature shows that many
authors used the terms introduced by the early scholars
(Hincks 1880 ; Jullien 1888 ; Levinsen 1902 , 1909 ; Canu and
Bassler 1920 ) rather arbitrarily, and there is much inconsistency in older taxonomic descriptions. Many taxonomists
still rely on the terminology and schematic illustrations of
Bassler ( 1953 ), who applied the terms of Levinsen ( 1902 ,
1909 ) to the schematics of Canu and Bassler ( 1920 ) (see
above). Ryland ( 1968 , 1970 , 1976 , 1979 ) and Ryland and
Hayward ( 1977 ) simplifi ed and improved the terminology,
stressing the main principles upon which such terminology
should be based (see Ostrovsky 2008b ). However, cheilostome brood chambers are very diverse, and in the absence of
a clear understanding of their internal structure, the situation
has been far from satisfactory. The terminology of the earlier
authors that later became standard has carried with it the
baggage of over-simplifi ed, even erroneous, ideas about
brood-chamber structure (discussed in Ostrovsky 2008b ).
As a result, taxonomists have continued to use the terms that
they prefer, which are often in contradiction with the actual
structure of the brood chamber.
An extensive review of cheilostome brooding structures
was recently published, aiming to correct this situation
(Ostrovsky 2008b ). It featured descriptions of the range of
different morphologies and a revision of terminology
commonly used in taxonomic descriptions. The traditional
morpho- functional terminological approach has been supplemented by a developmental approach. In the following
section, a revised and expanded version of this review is
presented.
Four main groups of embryo-incubation chambers are
known in Cheilostomata: (1) external membranous sacs
( Aetea , Eucratea loricata , “ Carbasea ” indivisa , Leiosalpinx
australis ); (2) skeletal (calcifi ed) chambers, including all
ovicells and brood chambers formed by spines (most cheilostomes); (3) internal brood sacs formed by non-calcifi ed
zooidal walls (in at least 22 families); and (4) female zooids
for intracoelomic incubation (Epistomiidae). This division is
based on wall composition and positioning of the brood
chamber (Ostrovsky 2008a , b ).
We still do not know how the chamber wall is formed in
the fi rst group and of what it consists (Fig. 2.52 ). Various
authors have suggested it to be an outgrowth of the introvert
wall, a cuticular chamber produced by the external cystid
wall or a sticky fertilization envelope (Stach 1938 ; Cook
1977b ; Ström 1977 ). In any case, the term “external membranous brood sac” should be applied to them all. Notably,
all cheilostomes possessing these sacs have simple skeletal
morphology and are considered to be less derived.
The second group covers the majority of incubation
chambers known in Cheilostomata. Apart from the acanthostegal brood chambers of Tendridae (“acanthostegous
ooecia” of Levinsen 1902 , 1909 ), which are represented by
2 Cheilostome Brood Chambers: Structure, Formation, Evolution