149
After studying anatomical sections of brooding A . anguina
Cook ( 1977b , p. 59) stated that the “brood chamber is
covered by a cuticular layer”, and that there was no opening
in sacs containing a developing embryo. In one population
of this species, she also described and illustrated a slight
proximal and ventral calcifi cation of the sac wall on the side
apposed to the zooidal wall, although it is not obvious if it
is actual calcifi cation in the only illustration published
(Fig. 2.52 , bottom). She suggested that the ovisac is a product
of the exterior zooidal wall, not an external diverticulum of
the tentacle sheath, since there is no tissue passing from the
zooidal opening to the sac. Finally, she noted that, in a signifi cant number of zooids, two embryos were simultaneously
contained within and released from the same brood sac.
A similar type of brooding in “transparent membranous
… ooecia … placed singly at the distal edge of the operculum” was recorded in Eucratea loricata (Eucrateidae) by
Eggleston ( 1963 , p. 29). This author also noted that “ooecia …
appear to extend into the zooidal cavity”, but his meaning is
unclear. In his following paper Eggleston ( 1972 , pp. 34–35)
added, “the embryos are brooded singly in membraneous
sacs above the orifi ce (as in Aetea spp.)” (see also Ryland and
Hayward 1977 ; Hayward and Ryland 1998 ). Stach ( 1938 ,
p. 397) discovered a similar type of external “brood-sac” in
malacostegan-like “ Carbasea ” indivisa (family incertae
sedis); each brooding zooid possesses 3–7 such sacs,
“developed from the distal portion of the tentacle- sheath
forming the inner wall of the operculum”. Larvae presumably escape from the sacs through a rupture of the wall.
Additionally, Gordon ( 1986 , p. 45) recorded “1–2 membranebounded embryos” attached to the frontal membrane
adjacent to the zooidal opening in Leiosalpinx australis
(Leiosalpingidae).
The lack of constancy in the position of the external
membranous sacs in Aetea (see above), the fact that they are
present during the reproductive period only (Winston 1982 )
as external fl exible transparent sacs without a cellular lining,
and the apparent lack of an opening appear to support the
suggestion of Levinsen ( 1909 ) and Ström ( 1977 ) that they
are a fertilization envelope. Formation of sticky fertilization
envelopes is known in a number of ctenostome brooders with
external embryonic incubation (see Sect. 3.4.4 ). Against this
idea is the partial calcifi cation of the sac wall reported by
Cook ( 1977b ) (Fig. 2.52 , bottom). Further study is necessary
to check both hypotheses, but if Levinsen and Ström are correct, this is the most primitive variant of external brooding in
cheilostomes, similar to that in some ctenostome bryozoans
(discussed in Chap. 3 ).
External membranous brood sacs thus occur in different
families and even suborders: Aetea (Aeteidae, suborder
Inovicellina), Eucratea and Leiosalpinx (Eucrateidae and
Leiosalpingidae, suborder Scrupariina), and “ Carbasea ”
indivisa (family and suborder incertae sedis). All the species
in these taxa have a simple anascan morphology, consistent
with the idea that their incubation chamber is actually a
fertilization envelope. Such a simple brooding mode might
be the most primitive form of parental care that, as in ctenostomes, could have evolved in primitive anascans de novo
or have been inherited from one or more ctenostome
ancestors. For example, in a paper proposing polyphyly in
Cheilostomata, Jebram ( 1992 ) conjectured that Aetea may be
related to Pottsiella -like ctenostomes, which also brood
embryos in external membranous sacs (Smith et al. 2003 ).
Another primitive trait in Aetea is a small setigerous collar in
the vestibulum, which, with few exceptions, is a ctenostome
character (reviewed in Prenant and Bobin 1966 ; Banta et al.
1995 ; McKinney and Dewel 2002 ). A recent molecular
analysis nested Aetea with primitive non-brooding (malacostegan) cheilostomes (Waeschenbach et al. 2012 ).
Despite their identical mode of brooding, the families
Aeteidae (Inovicellata), Eucrateidae and Leiosalpingidae
(Scrupariina) differ so much in zooidal morphology and the
time of their inferred stratigraphic origination, that it would
seem they acquired parental care independently. Further,
in addition to species with membranous sacs, suborder
Scrupariina currently includes genera with bilobate ovicells
( Scruparia and Brettiopsis ) (Scrupariidae). The question
arises if this clade is natural then (see also Eggleston 1972 ).
Molecular analysis should answer this question, but if yes,
then ovicells, as more complex and advanced brood chambers,
must have replaced membranous sacs in the evolution of
parental care in this clade. It would also mean that very different brood chambers evolved twice in Scrupariina.
2.4.2 Origin of Brooding in Cheilostomata:
Overview of the Major Hypotheses
According to Silén ( 1944 , p. 21), the earliest brood chamber
was an “embryo sack” or “embryonary” – an invagination of
the body wall of the egg-producing zooid formed by “extensive inward migration of ectodermic cells”. He considered
this invagination as “homologous to the polypide bud”
(p. 46). Later in evolution, the “embryo sack” moved towards
the zooidal opening, while two oral spines of the maternal
autozooid transformed to become an ooecium (Silén 1944 ,
1977 ; see also Ström 1977 ). This hypothesis was based on
the fi nding of a brood sac on the body wall of the ctenostome
Labiostomella gisleni , considered by Silén as a “protocheilostome” with many primitive characters (see also Silén 1942 ).
Santagata and Banta ( 1996 ) justly criticized Silén’s hypothesis as purely speculative in the absence of fossil evidence
and data on oviposition. We may note that Silén ( 1944 ) considered all bryozoan brood chambers as homologous, and
thus very ancient structures, interpreting the lack of brooding
in some Recent cheilostomes (Malacostega) as secondary.
2.4 Evolution of Brood Chambers in Cheilostomata
After studying anatomical sections of brooding A . anguina
Cook ( 1977b , p. 59) stated that the “brood chamber is
covered by a cuticular layer”, and that there was no opening
in sacs containing a developing embryo. In one population
of this species, she also described and illustrated a slight
proximal and ventral calcifi cation of the sac wall on the side
apposed to the zooidal wall, although it is not obvious if it
is actual calcifi cation in the only illustration published
(Fig. 2.52 , bottom). She suggested that the ovisac is a product
of the exterior zooidal wall, not an external diverticulum of
the tentacle sheath, since there is no tissue passing from the
zooidal opening to the sac. Finally, she noted that, in a signifi cant number of zooids, two embryos were simultaneously
contained within and released from the same brood sac.
A similar type of brooding in “transparent membranous
… ooecia … placed singly at the distal edge of the operculum” was recorded in Eucratea loricata (Eucrateidae) by
Eggleston ( 1963 , p. 29). This author also noted that “ooecia …
appear to extend into the zooidal cavity”, but his meaning is
unclear. In his following paper Eggleston ( 1972 , pp. 34–35)
added, “the embryos are brooded singly in membraneous
sacs above the orifi ce (as in Aetea spp.)” (see also Ryland and
Hayward 1977 ; Hayward and Ryland 1998 ). Stach ( 1938 ,
p. 397) discovered a similar type of external “brood-sac” in
malacostegan-like “ Carbasea ” indivisa (family incertae
sedis); each brooding zooid possesses 3–7 such sacs,
“developed from the distal portion of the tentacle- sheath
forming the inner wall of the operculum”. Larvae presumably escape from the sacs through a rupture of the wall.
Additionally, Gordon ( 1986 , p. 45) recorded “1–2 membranebounded embryos” attached to the frontal membrane
adjacent to the zooidal opening in Leiosalpinx australis
(Leiosalpingidae).
The lack of constancy in the position of the external
membranous sacs in Aetea (see above), the fact that they are
present during the reproductive period only (Winston 1982 )
as external fl exible transparent sacs without a cellular lining,
and the apparent lack of an opening appear to support the
suggestion of Levinsen ( 1909 ) and Ström ( 1977 ) that they
are a fertilization envelope. Formation of sticky fertilization
envelopes is known in a number of ctenostome brooders with
external embryonic incubation (see Sect. 3.4.4 ). Against this
idea is the partial calcifi cation of the sac wall reported by
Cook ( 1977b ) (Fig. 2.52 , bottom). Further study is necessary
to check both hypotheses, but if Levinsen and Ström are correct, this is the most primitive variant of external brooding in
cheilostomes, similar to that in some ctenostome bryozoans
(discussed in Chap. 3 ).
External membranous brood sacs thus occur in different
families and even suborders: Aetea (Aeteidae, suborder
Inovicellina), Eucratea and Leiosalpinx (Eucrateidae and
Leiosalpingidae, suborder Scrupariina), and “ Carbasea ”
indivisa (family and suborder incertae sedis). All the species
in these taxa have a simple anascan morphology, consistent
with the idea that their incubation chamber is actually a
fertilization envelope. Such a simple brooding mode might
be the most primitive form of parental care that, as in ctenostomes, could have evolved in primitive anascans de novo
or have been inherited from one or more ctenostome
ancestors. For example, in a paper proposing polyphyly in
Cheilostomata, Jebram ( 1992 ) conjectured that Aetea may be
related to Pottsiella -like ctenostomes, which also brood
embryos in external membranous sacs (Smith et al. 2003 ).
Another primitive trait in Aetea is a small setigerous collar in
the vestibulum, which, with few exceptions, is a ctenostome
character (reviewed in Prenant and Bobin 1966 ; Banta et al.
1995 ; McKinney and Dewel 2002 ). A recent molecular
analysis nested Aetea with primitive non-brooding (malacostegan) cheilostomes (Waeschenbach et al. 2012 ).
Despite their identical mode of brooding, the families
Aeteidae (Inovicellata), Eucrateidae and Leiosalpingidae
(Scrupariina) differ so much in zooidal morphology and the
time of their inferred stratigraphic origination, that it would
seem they acquired parental care independently. Further,
in addition to species with membranous sacs, suborder
Scrupariina currently includes genera with bilobate ovicells
( Scruparia and Brettiopsis ) (Scrupariidae). The question
arises if this clade is natural then (see also Eggleston 1972 ).
Molecular analysis should answer this question, but if yes,
then ovicells, as more complex and advanced brood chambers,
must have replaced membranous sacs in the evolution of
parental care in this clade. It would also mean that very different brood chambers evolved twice in Scrupariina.
2.4.2 Origin of Brooding in Cheilostomata:
Overview of the Major Hypotheses
According to Silén ( 1944 , p. 21), the earliest brood chamber
was an “embryo sack” or “embryonary” – an invagination of
the body wall of the egg-producing zooid formed by “extensive inward migration of ectodermic cells”. He considered
this invagination as “homologous to the polypide bud”
(p. 46). Later in evolution, the “embryo sack” moved towards
the zooidal opening, while two oral spines of the maternal
autozooid transformed to become an ooecium (Silén 1944 ,
1977 ; see also Ström 1977 ). This hypothesis was based on
the fi nding of a brood sac on the body wall of the ctenostome
Labiostomella gisleni , considered by Silén as a “protocheilostome” with many primitive characters (see also Silén 1942 ).
Santagata and Banta ( 1996 ) justly criticized Silén’s hypothesis as purely speculative in the absence of fossil evidence
and data on oviposition. We may note that Silén ( 1944 ) considered all bryozoan brood chambers as homologous, and
thus very ancient structures, interpreting the lack of brooding
in some Recent cheilostomes (Malacostega) as secondary.
2.4 Evolution of Brood Chambers in Cheilostomata