150
Santagata and Banta ( 1996 , p. 178) proposed an alternative hypothesis, according to which “vestibular brooding
preceded evolution of ovicells among cheilostomes.” They
suggested that, as in some ctenostomes, released zygotes stuck
to the everted vestibulum of the polypide in the hypothetical
“membraniporoid ancestor”, being withdrawn into its cavity
during polypide retraction. Embryo enlargement (as a result
of placental nutrition via the vestibular wall) fi nally led to the
removal of the embryo from the vestibulum. The latter was
still partially connected with the embryo and transformed to
the ooecial vesicle, phyletically accompanied by the origin
of a skeletal incubation chamber (ooecium). These authors
argued that the ooecium could have originated through
“excavation or evagination” of the “proximal end of the next
distal zooid” or/and modifi cation of its proximal spine(s) to
form the protective capsule (Santagata and Banta 1996 ,
p. 177). It was also suggested that internal incubation [in
internal brood sacs] evolved from vestibular incubation.
My own data and an analysis of the literature show that
the ideas of Santagata and Banta ( 1996 ) concerning the vestibulum as the original receptacle for embryon incubation are
based on a misinterpretation (Ostrovsky 2002 ; Taylor and
McKinney 2002 ; Ostrovsky et al. 2006 ); vestibular or introvert brooding is unknown in cheilostomes as is external
brooding accompanied by an everted vestibulum.
Dyrynda and King ( 1982 , p. 337), who worked with
Epistomia bursaria (Epistomiidae), suggested that the combination of intracoelomic incubation, “larval viviparity” and
a single polypide generation is primitive. In their opinion, the
subsequent origin of external brooding enabled polypide
recycling, thereby increasing fecundity. This idea is not supported by paleontological data, however. Moreover, if the
embryo is already protected by the zooid, the benefi ts of a
shift to external brooding are dubious. It is much more likely
that this mode of embryo incubation evolved secondarily
(see also Sect. 2.4.8 ).
A fourth hypothesis was suggested by Hughes ( 1987 ),
who thought that brood chambers were originally protective
structures that later assumed the function of extraembryonic
nutrition in some species. Hughes did not specify which
brood chambers, but, since he was studying ovicells, he
probably had them in mind. The variety of brood chambers,
their distribution among cheilostomes and fossil evidence
are supportive of this hypothesis. If true, the question arises,
how did the ooecium evolve?
Harmer ( 1902 ) suggested that it originated from two oral
spines of the maternal autozooid. Using Levinsen’s unpublished data on the structure of the bivalved ooecium in
Alysidium parasiticum , he speculated that ovicells were
formed from two expanded oral spines whose bases communicate with the maternal zooid. Levinsen ( 1902 ) himself fi rst
supported then later criticized this view, leaning towards the
idea that ovicells in Alysidium originate from two daughter
autozooids (Levinsen 1909 ). Supporting Harmer’s idea,
Silén ( 1944 , 1945 , 1977 ) offered in support the paired initial
calcifi cation of the ovicell fl oor (interpreted to be a rudiment
of allegedly lost spines) and the absence, in some species,
of the two disto-medial oral spines in maternal autozooids
initiating ooecium formation (see Harmelin 1973a ). It should
be noted that the latter argument is contradicted by the fact
that some smittinid and microporellid species retain the distalmost oral spines until the end of ooecium formation, after
which they break off or are resorbed (Soule 1973 ; Nielsen
1981 ) (see also Fig. 2.43D, F ).
My data fully support the idea that the ooecium originated
from modifi ed spines. Harmer ( 1902 ), who was the fi rst to
suggest it, emphasized the striking similarity between the
development of the ooecium and the frontal costae (modifi ed
spines) in Euthyroides episcopalis (discussed in Ostrovsky
1998 , 2002 ). Spines as the basis of ooecium formation have
been mentioned in several studies (Lang 1921 ; Larwood
1962 ; Ryland 1979 , 1982 ; Santagata and Banta 1996 ; discussed in Ostrovsky 1998 ). The critical factor, however, is
the zooid to which the ooecial spines belong. In the absence
of paleontological and new anatomical data, compromise
solutions were proposed. For instance, Ryland ( 1982 , p. 463)
wrote that the paired ooecial rudiment is formed at the
expense of the maternal zooid and the unpaired at the expense
of the distal zooid. In his opinion, this was associated with
the possible origin of the ooecium from paired maternal oral
spines in some species and from a “proximally situated
spinelike zooid” on the distal zooid in others.
The above data and paleontological evidence do not support the idea that the ooecium originated from two oral
spines. Instead, as Nielsen ( 1985 ) demonstrated, ooecium
formation from the distal zooid is fundamental in cheilostomes. Thus, ooecia are derivatives of spines developing on
the proximal wall of the distal zooid. Kenozooidal ooecia are
budded directly from the maternal autozooid when the distal
zooid is vestigialized (often accompanied by reduction of the
ooecial fold itself) (see Sect. 2.2 ).
Lang ( 1921 , p. xxxv) was the fi rst to state explicitly that
ooecia originate from modifi ed periopesial spines (i.e. of the
distal zooid): the “ovicell origin [in some cribrimorphs] from
costae is evident.” Larwood ( 1962 ) agreed. Santagata and
Banta ( 1996 ) suggested that in Bugula and Scrupocellaria
the ooecium may originate from one or a pair of proximal
spines [of the distal zooid]. Braiko ( 1967 ) and Santagata and
Banta ( 1996 ) also suggested that the acanthostegal brood
chambers of Tendra may represent a primitive stage in the
evolution of cribrimorph ovicells such as are found in
Figularia (a similar opinion was earlier expressed by
Reinhard 1875 ; see Sect. 2.1 ). Ostrovsky ( 2002 ) also considered this idea plausible, offering a detailed hypothetical
explanation of how the space between the spinocyst and the
frontal membrane of the distal zooid could be divided into a
2 Cheilostome Brood Chambers: Structure, Formation, Evolution
Santagata and Banta ( 1996 , p. 178) proposed an alternative hypothesis, according to which “vestibular brooding
preceded evolution of ovicells among cheilostomes.” They
suggested that, as in some ctenostomes, released zygotes stuck
to the everted vestibulum of the polypide in the hypothetical
“membraniporoid ancestor”, being withdrawn into its cavity
during polypide retraction. Embryo enlargement (as a result
of placental nutrition via the vestibular wall) fi nally led to the
removal of the embryo from the vestibulum. The latter was
still partially connected with the embryo and transformed to
the ooecial vesicle, phyletically accompanied by the origin
of a skeletal incubation chamber (ooecium). These authors
argued that the ooecium could have originated through
“excavation or evagination” of the “proximal end of the next
distal zooid” or/and modifi cation of its proximal spine(s) to
form the protective capsule (Santagata and Banta 1996 ,
p. 177). It was also suggested that internal incubation [in
internal brood sacs] evolved from vestibular incubation.
My own data and an analysis of the literature show that
the ideas of Santagata and Banta ( 1996 ) concerning the vestibulum as the original receptacle for embryon incubation are
based on a misinterpretation (Ostrovsky 2002 ; Taylor and
McKinney 2002 ; Ostrovsky et al. 2006 ); vestibular or introvert brooding is unknown in cheilostomes as is external
brooding accompanied by an everted vestibulum.
Dyrynda and King ( 1982 , p. 337), who worked with
Epistomia bursaria (Epistomiidae), suggested that the combination of intracoelomic incubation, “larval viviparity” and
a single polypide generation is primitive. In their opinion, the
subsequent origin of external brooding enabled polypide
recycling, thereby increasing fecundity. This idea is not supported by paleontological data, however. Moreover, if the
embryo is already protected by the zooid, the benefi ts of a
shift to external brooding are dubious. It is much more likely
that this mode of embryo incubation evolved secondarily
(see also Sect. 2.4.8 ).
A fourth hypothesis was suggested by Hughes ( 1987 ),
who thought that brood chambers were originally protective
structures that later assumed the function of extraembryonic
nutrition in some species. Hughes did not specify which
brood chambers, but, since he was studying ovicells, he
probably had them in mind. The variety of brood chambers,
their distribution among cheilostomes and fossil evidence
are supportive of this hypothesis. If true, the question arises,
how did the ooecium evolve?
Harmer ( 1902 ) suggested that it originated from two oral
spines of the maternal autozooid. Using Levinsen’s unpublished data on the structure of the bivalved ooecium in
Alysidium parasiticum , he speculated that ovicells were
formed from two expanded oral spines whose bases communicate with the maternal zooid. Levinsen ( 1902 ) himself fi rst
supported then later criticized this view, leaning towards the
idea that ovicells in Alysidium originate from two daughter
autozooids (Levinsen 1909 ). Supporting Harmer’s idea,
Silén ( 1944 , 1945 , 1977 ) offered in support the paired initial
calcifi cation of the ovicell fl oor (interpreted to be a rudiment
of allegedly lost spines) and the absence, in some species,
of the two disto-medial oral spines in maternal autozooids
initiating ooecium formation (see Harmelin 1973a ). It should
be noted that the latter argument is contradicted by the fact
that some smittinid and microporellid species retain the distalmost oral spines until the end of ooecium formation, after
which they break off or are resorbed (Soule 1973 ; Nielsen
1981 ) (see also Fig. 2.43D, F ).
My data fully support the idea that the ooecium originated
from modifi ed spines. Harmer ( 1902 ), who was the fi rst to
suggest it, emphasized the striking similarity between the
development of the ooecium and the frontal costae (modifi ed
spines) in Euthyroides episcopalis (discussed in Ostrovsky
1998 , 2002 ). Spines as the basis of ooecium formation have
been mentioned in several studies (Lang 1921 ; Larwood
1962 ; Ryland 1979 , 1982 ; Santagata and Banta 1996 ; discussed in Ostrovsky 1998 ). The critical factor, however, is
the zooid to which the ooecial spines belong. In the absence
of paleontological and new anatomical data, compromise
solutions were proposed. For instance, Ryland ( 1982 , p. 463)
wrote that the paired ooecial rudiment is formed at the
expense of the maternal zooid and the unpaired at the expense
of the distal zooid. In his opinion, this was associated with
the possible origin of the ooecium from paired maternal oral
spines in some species and from a “proximally situated
spinelike zooid” on the distal zooid in others.
The above data and paleontological evidence do not support the idea that the ooecium originated from two oral
spines. Instead, as Nielsen ( 1985 ) demonstrated, ooecium
formation from the distal zooid is fundamental in cheilostomes. Thus, ooecia are derivatives of spines developing on
the proximal wall of the distal zooid. Kenozooidal ooecia are
budded directly from the maternal autozooid when the distal
zooid is vestigialized (often accompanied by reduction of the
ooecial fold itself) (see Sect. 2.2 ).
Lang ( 1921 , p. xxxv) was the fi rst to state explicitly that
ooecia originate from modifi ed periopesial spines (i.e. of the
distal zooid): the “ovicell origin [in some cribrimorphs] from
costae is evident.” Larwood ( 1962 ) agreed. Santagata and
Banta ( 1996 ) suggested that in Bugula and Scrupocellaria
the ooecium may originate from one or a pair of proximal
spines [of the distal zooid]. Braiko ( 1967 ) and Santagata and
Banta ( 1996 ) also suggested that the acanthostegal brood
chambers of Tendra may represent a primitive stage in the
evolution of cribrimorph ovicells such as are found in
Figularia (a similar opinion was earlier expressed by
Reinhard 1875 ; see Sect. 2.1 ). Ostrovsky ( 2002 ) also considered this idea plausible, offering a detailed hypothetical
explanation of how the space between the spinocyst and the
frontal membrane of the distal zooid could be divided into a
2 Cheilostome Brood Chambers: Structure, Formation, Evolution