158
maternal zooid) isolates the brood cavity from the external
medium and, in the case of matrotrophic species, also ensures
extraembryonic nutrition.
In most ovicellate cheilostomes, this complex is formed
by two successively budding zooids. At the same time, in
Monoporellidae, the non-calcifi ed frontal walls of the two
distolateral zooids that close the lateral foramina play an
important role in the isolation of the brood cavity from the
environment. In this way, the maternal, distal and neighbouring zooids are combined into a “cluster of polymorphic autozooids forming [the] brooding structure” (Cheetham and
Cook 1983 , p. 166, fi g. 72.2; Ostrovsky and Taylor 2005a ;
see also Sect. 2.4.5 ). In Cellariidae the brood cavity is limited by the walls of 2–3 distal and/or distolateral zooids, and
so the entire complex consists of 3–4 zooids. Similar cormidia independently evolved in Heterooecium (Tendridae). Its
acanthostegal brood chambers comprise an egg-producing
autozooidal polymorph and a distal kenozooid that forms a
costate brood chamber.
Interestingly, the highest level of integration associated
with the formation of brooding structures can be found in
some rectangulate Cyclostomata, in which large, colonial
brood chambers occur (Borg 1926 ; Beklemishev 1969 ;
Schäfer 1991 ; Reed 1991 ).
2.4.8.2 Reduction of Ectooecial Calcifi cation
Levinsen ( 1909 ) was the fi rst to pay attention to differences
in ooecial-wall calcifi cation in cheilostomes. For instance, in
Callopora there are species with a completely calcifi ed
ectooecium ( C . minuta , see Harmelin 1973b ) and species in
which it is mostly membranous with only the base calcifi ed
( C . dumerilii ; see Levinsen 1909 ; Prenant and Bobin 1966 ;
Zabala and Maluquer 1988 ; Ostrovsky and Schäfer 2003 ;
Ostrovsky et al. 2003 , 2009a ). While the early calloporids
Wilbertopora and Gilbertopora have a completely calcifi ed
ooecium, most Recent calloporids have cuticular windows of
different sizes and shapes in their ooecia. Analysis of the literature and my own data show that most cheilostome families are characterized by some degree of reduction of ooecial
calcifi cation. This reduction is expressed as membranous
windows or pseudopores or as a complete loss of calcifi cation of the ectooecium, which then often becomes a direct
continuation of the non-calcifi ed frontal membrane of the
distal zooid (in escharelliform and microporelliform ooecia).
All these facts indicate the presence of an evolutionary trend
towards gradual reduction of ectooecial calcifi cation,
expressed within the order Cheilostomata independently in
several distant lineages.
Such an evolutionary trend begs the question of the biological expedience of lessening of the mechanical strength of
a protective structure. Calcifi cation has an energetic cost and
reducing it can be an advantageous trade-off in favour of
some other benefi t. Inter alia, the formation of ovicells
increases overall colony volume and existing non-calcifi ed
surfaces may become insuffi cient for normal gas exchange.
Cuticular windows in ooecia might mitigate this negative
aspect, an idea indirectly supported by the fact that secondary
calcifi cation, characteristic of many cheilostomes, does
not typically overgrow non-calcifi ed ooecial areas such as
pseudopores and membranous windows; for example, in
Smittinidae, Umbonulidae (Fig. 2.41A ) and Bitectiporidae
secondary calcifi cation does not close the ovicell roof where
pseudopores are located. Signifi cantly, Navarrete et al. ( 2005 )
noted a latitudinal trend in the number of pseudopores in the
ovicells of Celleporella species along the Chilean coast, suggesting that the north–south decline was modulated in relation to temperature and dissolved oxygen.
Levinsen ( 1909 ) noted that the calcifi ed entooecium is
usually thicker in species with a membranous ectooecium
and my data would seem to confi rm this. In such cases, ooecial structure is like that of a frontal zooidal shield with a
hypostegal coelom (Sandberg 1977 ). Such shields are developed in a majority of cheilostome species, even though the
outer (frontal) wall is non-calcifi ed, and it is apparent that
such an arrangement must be advantageous. [Inter alia, it
allows for the possibility of frontal budding and colony
strengthening (Gordon and Voigt 1996 ).] Since the gap
between the outer membraneous wall and the underlying
skeletal wall is very small, the whole construction has a high
assurance factor. The pressure exercised upon the surface of
such a frontal complex would be instantly transmitted to the
calcifi ed wall. At the same time, gas exchange is not hindered in any way. The situation in ovicells may be analogous
(Figs. 2.34 , 2.36 , 2.44 , and 2.45 ) (Ostrovsky et al. 2009a ).
2.4.8.3 Reduction of the Distal OoeciumProducing Zooid
This trend in brood-chamber evolution culminated in terminal ovicells and kenozooidal ooecia; (1) In the former case
the ooecium is formed by the distal kenozooid, which constitutes the base of the brood chamber. The distally protruding
part of the kenozooid is absent (Figs. 1.30B , 1.36 , 2.6a (C, E),
b (D, F), 2.23 , and 2.42 ). (2) In the latter case the only part of
the distal kenozooid remaining in kenozooidal ooecia is a
small area (the originating “chamber”) at the site of contact
with the maternal autozooid (Figs. 1.22 , 1.25A , 2.6a (D),
b (A–C, E), 2.7b (C), 2.25B , and 2.29 ).
In many cheilostome genera and families, terminal ovicells co-occur with ooecia formed by distal autozooids,
kenozooids (with the distal part protruding) and avicularia.
Moreover, ovicells of two different categories may be
found within a single species or colony (in Cribrilina
punctata , Puellina harmeri , Callopora craticula ) (see
Levinsen 1909 ; Ristedt 1985 ; Harmelin and Arístegui
1988 ; Bishop 1994 ; Ostrovsky et al. 2009a ). In some other
taxa the ooecia are always formed by the distal kenozooid
2 Cheilostome Brood Chambers: Structure, Formation, Evolution
maternal zooid) isolates the brood cavity from the external
medium and, in the case of matrotrophic species, also ensures
extraembryonic nutrition.
In most ovicellate cheilostomes, this complex is formed
by two successively budding zooids. At the same time, in
Monoporellidae, the non-calcifi ed frontal walls of the two
distolateral zooids that close the lateral foramina play an
important role in the isolation of the brood cavity from the
environment. In this way, the maternal, distal and neighbouring zooids are combined into a “cluster of polymorphic autozooids forming [the] brooding structure” (Cheetham and
Cook 1983 , p. 166, fi g. 72.2; Ostrovsky and Taylor 2005a ;
see also Sect. 2.4.5 ). In Cellariidae the brood cavity is limited by the walls of 2–3 distal and/or distolateral zooids, and
so the entire complex consists of 3–4 zooids. Similar cormidia independently evolved in Heterooecium (Tendridae). Its
acanthostegal brood chambers comprise an egg-producing
autozooidal polymorph and a distal kenozooid that forms a
costate brood chamber.
Interestingly, the highest level of integration associated
with the formation of brooding structures can be found in
some rectangulate Cyclostomata, in which large, colonial
brood chambers occur (Borg 1926 ; Beklemishev 1969 ;
Schäfer 1991 ; Reed 1991 ).
2.4.8.2 Reduction of Ectooecial Calcifi cation
Levinsen ( 1909 ) was the fi rst to pay attention to differences
in ooecial-wall calcifi cation in cheilostomes. For instance, in
Callopora there are species with a completely calcifi ed
ectooecium ( C . minuta , see Harmelin 1973b ) and species in
which it is mostly membranous with only the base calcifi ed
( C . dumerilii ; see Levinsen 1909 ; Prenant and Bobin 1966 ;
Zabala and Maluquer 1988 ; Ostrovsky and Schäfer 2003 ;
Ostrovsky et al. 2003 , 2009a ). While the early calloporids
Wilbertopora and Gilbertopora have a completely calcifi ed
ooecium, most Recent calloporids have cuticular windows of
different sizes and shapes in their ooecia. Analysis of the literature and my own data show that most cheilostome families are characterized by some degree of reduction of ooecial
calcifi cation. This reduction is expressed as membranous
windows or pseudopores or as a complete loss of calcifi cation of the ectooecium, which then often becomes a direct
continuation of the non-calcifi ed frontal membrane of the
distal zooid (in escharelliform and microporelliform ooecia).
All these facts indicate the presence of an evolutionary trend
towards gradual reduction of ectooecial calcifi cation,
expressed within the order Cheilostomata independently in
several distant lineages.
Such an evolutionary trend begs the question of the biological expedience of lessening of the mechanical strength of
a protective structure. Calcifi cation has an energetic cost and
reducing it can be an advantageous trade-off in favour of
some other benefi t. Inter alia, the formation of ovicells
increases overall colony volume and existing non-calcifi ed
surfaces may become insuffi cient for normal gas exchange.
Cuticular windows in ooecia might mitigate this negative
aspect, an idea indirectly supported by the fact that secondary
calcifi cation, characteristic of many cheilostomes, does
not typically overgrow non-calcifi ed ooecial areas such as
pseudopores and membranous windows; for example, in
Smittinidae, Umbonulidae (Fig. 2.41A ) and Bitectiporidae
secondary calcifi cation does not close the ovicell roof where
pseudopores are located. Signifi cantly, Navarrete et al. ( 2005 )
noted a latitudinal trend in the number of pseudopores in the
ovicells of Celleporella species along the Chilean coast, suggesting that the north–south decline was modulated in relation to temperature and dissolved oxygen.
Levinsen ( 1909 ) noted that the calcifi ed entooecium is
usually thicker in species with a membranous ectooecium
and my data would seem to confi rm this. In such cases, ooecial structure is like that of a frontal zooidal shield with a
hypostegal coelom (Sandberg 1977 ). Such shields are developed in a majority of cheilostome species, even though the
outer (frontal) wall is non-calcifi ed, and it is apparent that
such an arrangement must be advantageous. [Inter alia, it
allows for the possibility of frontal budding and colony
strengthening (Gordon and Voigt 1996 ).] Since the gap
between the outer membraneous wall and the underlying
skeletal wall is very small, the whole construction has a high
assurance factor. The pressure exercised upon the surface of
such a frontal complex would be instantly transmitted to the
calcifi ed wall. At the same time, gas exchange is not hindered in any way. The situation in ovicells may be analogous
(Figs. 2.34 , 2.36 , 2.44 , and 2.45 ) (Ostrovsky et al. 2009a ).
2.4.8.3 Reduction of the Distal OoeciumProducing Zooid
This trend in brood-chamber evolution culminated in terminal ovicells and kenozooidal ooecia; (1) In the former case
the ooecium is formed by the distal kenozooid, which constitutes the base of the brood chamber. The distally protruding
part of the kenozooid is absent (Figs. 1.30B , 1.36 , 2.6a (C, E),
b (D, F), 2.23 , and 2.42 ). (2) In the latter case the only part of
the distal kenozooid remaining in kenozooidal ooecia is a
small area (the originating “chamber”) at the site of contact
with the maternal autozooid (Figs. 1.22 , 1.25A , 2.6a (D),
b (A–C, E), 2.7b (C), 2.25B , and 2.29 ).
In many cheilostome genera and families, terminal ovicells co-occur with ooecia formed by distal autozooids,
kenozooids (with the distal part protruding) and avicularia.
Moreover, ovicells of two different categories may be
found within a single species or colony (in Cribrilina
punctata , Puellina harmeri , Callopora craticula ) (see
Levinsen 1909 ; Ristedt 1985 ; Harmelin and Arístegui
1988 ; Bishop 1994 ; Ostrovsky et al. 2009a ). In some other
taxa the ooecia are always formed by the distal kenozooid
2 Cheilostome Brood Chambers: Structure, Formation, Evolution