162
Internal brood sacs are the only incubational structures in
the Cupuladriidae (Ostrovsky et al. 2009b ), Chlidoniidae
(Waters 1913 ; Harmer 1926 ; Ostrovsky, unpublished data),
Steginoporellidae (Waters 1913 ; Marcus 1922 ; Harmer
1926 ; Osburn 1950 ), Pasytheidae (Gordon 1984 ), Adeonidae
(Waters 1912 , 1913 ), Exechonellidae (Fransen 1986 ),
Watersiporidae (Waters 1912 ; Mawatari 1952 ), Cryptosulidae
(Calvet 1900 ) and Inversiulidae (Gordon 1984 ; Hayward
1995 ). In most of these taxa the presence of brood sacs was
registered in studies made on live or fi xed (wet) colonies
with embryos or else in studies involving anatomical sections (Fig. 2.47 ). For the others, the existence of brood sacs
is only inferred. For instance, all species and genera of
Bryopastoridae, Euthyrisellidae and Didymosellidae are
thought to have internal brooding in “ovisacs” of zooidal
polymorphs (Cook 1979 ; Cook and Chimonides 1981b ;
Gordon 1986 ; Zabala and Maluquer 1988 ). There are no data
on the brooding structures in a number of genera (see above)
including Carbasea carbasea (Flustridae), the fi rst cheilostome reported to have internal brooding (Grant 1827 ; Zabala
and Maluquer 1988 ; Ostrovsky et al. 2006 , 2008 ).
Internal brood sacs could have evolved as modifi cations
of ovicells, endozooidal as well as immersed. This possibility is supported by the fact that, in species with brood
sacs (e.g. Cauloramphus , Beania bilaminata , Nematofl ustra
fl agellata and Reciprocus regalis ), the ooecial vesicle is
retained, together with its sclerite and musculature.
Whatever the ovicell type was, the origin of internal brood
sacs should have been accompanied by reduction of the
calcifi ed fl oor of the brood cavity, invagination of the distal wall of the maternal zooid and disappearance of the
ooecium. A strongly reduced ooecium is retained in species with immersed ovicells ( Crassimarginatella sp.,
Bugulopsis monotrypa and some others) and with brood
sacs ( Cauloramphus , Beania ). In most fl ustrids, the brood
cavity of endozooidal ovicells lies in the proximal part of
the distal autozooid. In contrast, the internal brood sacs of
Nematofl ustra fl agellata and “ Bifl ustra ” perfragilis lie in
the distal half of the maternal zooid (Fig. 2.46A, B ). Thus,
immersion of the brood cavity in fl ustrids should have
been accompanied by its proximal displacement and a
change in the position of its opening.
The structure of the internal brood sac in the presumed
calloporid Gontarella sp. is almost identical to that in the
calloporid Cauloramphus (compare Figs. 2.25B and 2.46C ).
This variant could be the result of complete reduction of the
ooecium. On the other hand, modifi cation of immersed ovicells, as in Crassimarginatella sp., could have brought about
the same result. Thus, even within the Calloporidae, the transition to internal brooding may have been achieved in different ways (Ostrovsky et al. 2006 , 2009a ).
It seems evident that immersion of the incubation chamber is associated with better protection of the developing
embryo – immersed and endozooidal ovicells are less
exposed than other ovicells and thus less likely to be damaged. On the other hand, the reduction and even complete
disappearance of the calcifi ed ooecial roof may be thought to
decrease protection of the embryo. In an attempt to explain
this phenomenon, Hastings ( 1964 ) looked for correlations
between the presence or absence of ovicells within the same
genus and for differences in vertical, geographical and
climatic distribution of species, but failed to fi nd any.
Eggleston ( 1972 ) noted that internal brooding is characteristic of intertidal species and suggested the embryos of such
species might be better protected against exposure to air than
in species with ovicells.
Having studied internal brooding anatomically, I have
suggested several other alternative or complementary scenarios (Ostrovsky et al. 2006 , 2009b ):
1. Since ovicell formation requires considerable amounts of
materials and energy, reduction of the ooecium and associated structures could release some resources for somatic
growth. The result could be a higher growth rate or
enlargement of the colony.
2. The zooid cavity is more capacious than the ovicell, and a
large zooid has enough room for a large larva, which is
likely to be more competitive after settlement. Therefore,
a transition to internal brooding might be associated with
the acquisition of a larger larva. In the Adeonidae, the
transition to internal brooding appears to have caused the
origin of female zooidal polymorphs.
3. Internal brooding may have been an evolutionary response
to predators feeding on embryos contained in ovicells
(such as acleithral). Small species of nudibranchs and
pycnogonids have been shown to feed on individual
zooids (McBeth 1968 ; Wyer and King 1973 ; Lidgard
2008a , b ; reviewed in McKinney et al. 2003 ).
Santagata and Banta ( 1996 ) suggested that the internal
brood sac is a modifi cation of the expanded vestibulum, and
internal brooding was the initial mode of incubation in the
Cheilostomata (see Sect. 2.4.2 ). Ryland ( 1970 , p. 95) also
proposed that “incubation in an embryo sac suspended in the
coelom might have been the primitive arrangement”. The
geological record does not support these hypotheses; species
with internal brooding mostly emerged in the Middle Eocene
and later. For instance, Watersipora and Cryptosula appeared
in the Late Miocene. A much more ancient brooding type
was incubation in a cage-like hyperstomial ovicell made of
spines formed by the distal autozooid (Taylor and McKinney
2002 ; Ostrovsky and Taylor 2004 , 2005a ). It is much easier
to interpret internal brooding as the fi nal stage of the transition from hyperstomial to endozooidal and immersed ovicells,
2 Cheilostome Brood Chambers: Structure, Formation, Evolution
Internal brood sacs are the only incubational structures in
the Cupuladriidae (Ostrovsky et al. 2009b ), Chlidoniidae
(Waters 1913 ; Harmer 1926 ; Ostrovsky, unpublished data),
Steginoporellidae (Waters 1913 ; Marcus 1922 ; Harmer
1926 ; Osburn 1950 ), Pasytheidae (Gordon 1984 ), Adeonidae
(Waters 1912 , 1913 ), Exechonellidae (Fransen 1986 ),
Watersiporidae (Waters 1912 ; Mawatari 1952 ), Cryptosulidae
(Calvet 1900 ) and Inversiulidae (Gordon 1984 ; Hayward
1995 ). In most of these taxa the presence of brood sacs was
registered in studies made on live or fi xed (wet) colonies
with embryos or else in studies involving anatomical sections (Fig. 2.47 ). For the others, the existence of brood sacs
is only inferred. For instance, all species and genera of
Bryopastoridae, Euthyrisellidae and Didymosellidae are
thought to have internal brooding in “ovisacs” of zooidal
polymorphs (Cook 1979 ; Cook and Chimonides 1981b ;
Gordon 1986 ; Zabala and Maluquer 1988 ). There are no data
on the brooding structures in a number of genera (see above)
including Carbasea carbasea (Flustridae), the fi rst cheilostome reported to have internal brooding (Grant 1827 ; Zabala
and Maluquer 1988 ; Ostrovsky et al. 2006 , 2008 ).
Internal brood sacs could have evolved as modifi cations
of ovicells, endozooidal as well as immersed. This possibility is supported by the fact that, in species with brood
sacs (e.g. Cauloramphus , Beania bilaminata , Nematofl ustra
fl agellata and Reciprocus regalis ), the ooecial vesicle is
retained, together with its sclerite and musculature.
Whatever the ovicell type was, the origin of internal brood
sacs should have been accompanied by reduction of the
calcifi ed fl oor of the brood cavity, invagination of the distal wall of the maternal zooid and disappearance of the
ooecium. A strongly reduced ooecium is retained in species with immersed ovicells ( Crassimarginatella sp.,
Bugulopsis monotrypa and some others) and with brood
sacs ( Cauloramphus , Beania ). In most fl ustrids, the brood
cavity of endozooidal ovicells lies in the proximal part of
the distal autozooid. In contrast, the internal brood sacs of
Nematofl ustra fl agellata and “ Bifl ustra ” perfragilis lie in
the distal half of the maternal zooid (Fig. 2.46A, B ). Thus,
immersion of the brood cavity in fl ustrids should have
been accompanied by its proximal displacement and a
change in the position of its opening.
The structure of the internal brood sac in the presumed
calloporid Gontarella sp. is almost identical to that in the
calloporid Cauloramphus (compare Figs. 2.25B and 2.46C ).
This variant could be the result of complete reduction of the
ooecium. On the other hand, modifi cation of immersed ovicells, as in Crassimarginatella sp., could have brought about
the same result. Thus, even within the Calloporidae, the transition to internal brooding may have been achieved in different ways (Ostrovsky et al. 2006 , 2009a ).
It seems evident that immersion of the incubation chamber is associated with better protection of the developing
embryo – immersed and endozooidal ovicells are less
exposed than other ovicells and thus less likely to be damaged. On the other hand, the reduction and even complete
disappearance of the calcifi ed ooecial roof may be thought to
decrease protection of the embryo. In an attempt to explain
this phenomenon, Hastings ( 1964 ) looked for correlations
between the presence or absence of ovicells within the same
genus and for differences in vertical, geographical and
climatic distribution of species, but failed to fi nd any.
Eggleston ( 1972 ) noted that internal brooding is characteristic of intertidal species and suggested the embryos of such
species might be better protected against exposure to air than
in species with ovicells.
Having studied internal brooding anatomically, I have
suggested several other alternative or complementary scenarios (Ostrovsky et al. 2006 , 2009b ):
1. Since ovicell formation requires considerable amounts of
materials and energy, reduction of the ooecium and associated structures could release some resources for somatic
growth. The result could be a higher growth rate or
enlargement of the colony.
2. The zooid cavity is more capacious than the ovicell, and a
large zooid has enough room for a large larva, which is
likely to be more competitive after settlement. Therefore,
a transition to internal brooding might be associated with
the acquisition of a larger larva. In the Adeonidae, the
transition to internal brooding appears to have caused the
origin of female zooidal polymorphs.
3. Internal brooding may have been an evolutionary response
to predators feeding on embryos contained in ovicells
(such as acleithral). Small species of nudibranchs and
pycnogonids have been shown to feed on individual
zooids (McBeth 1968 ; Wyer and King 1973 ; Lidgard
2008a , b ; reviewed in McKinney et al. 2003 ).
Santagata and Banta ( 1996 ) suggested that the internal
brood sac is a modifi cation of the expanded vestibulum, and
internal brooding was the initial mode of incubation in the
Cheilostomata (see Sect. 2.4.2 ). Ryland ( 1970 , p. 95) also
proposed that “incubation in an embryo sac suspended in the
coelom might have been the primitive arrangement”. The
geological record does not support these hypotheses; species
with internal brooding mostly emerged in the Middle Eocene
and later. For instance, Watersipora and Cryptosula appeared
in the Late Miocene. A much more ancient brooding type
was incubation in a cage-like hyperstomial ovicell made of
spines formed by the distal autozooid (Taylor and McKinney
2002 ; Ostrovsky and Taylor 2004 , 2005a ). It is much easier
to interpret internal brooding as the fi nal stage of the transition from hyperstomial to endozooidal and immersed ovicells,
2 Cheilostome Brood Chambers: Structure, Formation, Evolution