148
This prominent researcher studied whole, sectioned and
developing ovicells in more than 80 cheilostome species in
62 genera, but, since he mostly worked with cleaned bryozoan skeletons, his conclusions can be misleading (discussed
in Silén 1945 ; Woollacott and Zimmer 1972a ; Ostrovsky
2009 ). As a result, Levinsen’s results have been rarely used,
and careful restudy of these species is necessary. Ovicell
anatomy should also be reinvestigated in some recently
studied species. For instance, Nielsen’s ( 1981 ) schematic of
Fenestrulina miramara (as F . malusii ), based only on the
skeleton, differs from that presented Calvet ( 1900 , fi g. 21) in
Fenestrulina malusii (as Microporella ) based on decalcifi ed
sections. My data on Fenestrulina (see above) do not contradict these papers, but better, fi xed material is required to
draw defi nitive conclusions.
2.4
Evolution of Brood Chambers
in Cheilostomata
The vast structural diversity of incubational chambers in
cheilostome bryozoans led researchers to believe that these
structures are not homologous in different cheilostome
groups and that their similarities could be explained by convergence (Harmer 1926 ; Osburn 1950 ; Ryland 1974 ; Cook
1979 ; Cook and Hayward 1983 ; Reed 1991 ; Santagata and
Banta 1996 ; see also Taylor 1988 ). If so, the questions to be
answered are: How many times, when and in which lineages did embryo incubation evolve? How did different
brood-chamber types evolve in cheilostomes and what were
the main trends during their further transformation?
2.4.1 External Membranous Brood Sacs
The simplest brood chambers are external membranous
sacs, although the questions surrounding their origin and
wall composition are still open. Waters ( 1896 [1898] , p. 4,
pl. 1, fi gs. 1–3, 1913 , pl. 64, fi g. 1) discovered them (calling
“ovicells”) in Aetea sica (as A. anguina forma recta ) and A .
anguina , depicting them on top of the dorsal side of the
erect portion in autozooids. In contrast, Robertson ( 1905 , p.
246) recorded a “membranous bag”, situated “on the ventral side” of the zooid “below the operculum but exterior to
the aperture” in A . anguina . She suggested that the curvature of the tubular part of the zooid “afford[s]… protection
to the delicate ooecium and its contents”. In considering the
“great transparency” and position of this brooding structure, Levinsen ( 1909 , p. 93), concluded that “the supposed
ovicellular wall [is] only … a shell membrane surrounding
the egg,” a view accepted by Ström ( 1977 ). Waters ( 1913 )
challenged it, saying that the position of all the brood sacs
he saw was consistent. He referred to Osburn ( 1912 ), who
also depicted the brood sacs at the top of the autozooid,
distal to the operculum in A . anguina . Waters ( 1913 , p. 464)
additionally wrote: “One section shows the zooecial wall
bulging out and the ovum partly in this portion, which is the
commencement of the ovicell.” Although membranous
brood sacs have nothing to do with true ovicells, this observation is in accord with the later suggestion of Cheetham
(personal communication in Cook 1977b ) that this sac
might be an outgrowth of the cystid wall with a coelomic
space inside.
Further researchers have supported both opinions on the
position of these “ooecia” or “ovisacs”. It has been described
as attached to the frontal membrane proximal to the operculum (Marcus 1937 ; Hastings 1943 , pp. 471–472; Gautier
1962 , p. 27; Mawatari 1973b , p. 413) and to the dorsal side
(Marcus 1940 , pp. 103–105; Cook 1968b , p. 137, 1977b ,
1985 ) (reviewed in Prenant and Bobin 1966 and Cook
1968b ). Problematically, all of the above authors have
described the “ovisac” as either proximal or distal in the
same species, Aetea anguina (see also Ryland and Hayward
1977 ; Cook 1985 ). Cook ( 1968b , p. 137) stressed that “the
occurrence of ovisacs either in the dorsal or ventral position
is remarkably consistent in the populations where they are
abundant,” suggesting also that different authors may in
fact have been dealing with different species. For instance,
among more than 100 membranous sacs studied by Cook
( 1968b , fi g. 2D), all were dorsal, though asymmetrical
(dorsal or dorsolateral). Occhipinti Ambrogi ( 1981 )
described these sacs as situated either proximal or distal to
the operculum in A . anguina (also cited in Hayward and
Ryland 1998 ). Both positions are also reported in A . sica
(summarized in Ryland and Hayward 1977 ; Hayward and
Ryland 1998 ; see also Prenant and Bobin 1966 ).
Hastings ( 1943 ) noted that sacs containing an early
embryo were closely applied to the zooidal frontal membrane, whereas those with an advanced embryo were attached
to the membrane by a narrow distal zone that is also evident
in empty sacs (1943, fi g. 57). Similarly, a narrow basal part
of “the membranous ovicelligeous sac” was described and
depicted by Mawatari ( 1973b , p. 414, fi g. 1E, F). Also
Hayward and Ryland ( 1998 , p. 100) wrote that those “ovisacs”
that were situated proximal to the autozooidal orifi ce were at
fi rst appressed to the frontal membrane, but later became free
except for an attachment site proximal to the operculum.
According to Cook ( 1977b , p. 59), the sac is “closely apposed
to the dorsal part of the zooid body wall but attached only in
its distal end.”
Interestingly, Mawatari ( 1973b , p. 414) misinterpreted
Busk ( 1849 , but mistakenly referenced as 1884 ) as having
observed a “membranous ovicelligeous sac” in Aetea , comparing it with “the bag of the pelicans beak”. Busk’s ( 1849 ,
p. 125) text in fact speaks of the membranous frontal wall in
this way, not the brood sac.
2 Cheilostome Brood Chambers: Structure, Formation, Evolution
This prominent researcher studied whole, sectioned and
developing ovicells in more than 80 cheilostome species in
62 genera, but, since he mostly worked with cleaned bryozoan skeletons, his conclusions can be misleading (discussed
in Silén 1945 ; Woollacott and Zimmer 1972a ; Ostrovsky
2009 ). As a result, Levinsen’s results have been rarely used,
and careful restudy of these species is necessary. Ovicell
anatomy should also be reinvestigated in some recently
studied species. For instance, Nielsen’s ( 1981 ) schematic of
Fenestrulina miramara (as F . malusii ), based only on the
skeleton, differs from that presented Calvet ( 1900 , fi g. 21) in
Fenestrulina malusii (as Microporella ) based on decalcifi ed
sections. My data on Fenestrulina (see above) do not contradict these papers, but better, fi xed material is required to
draw defi nitive conclusions.
2.4
Evolution of Brood Chambers
in Cheilostomata
The vast structural diversity of incubational chambers in
cheilostome bryozoans led researchers to believe that these
structures are not homologous in different cheilostome
groups and that their similarities could be explained by convergence (Harmer 1926 ; Osburn 1950 ; Ryland 1974 ; Cook
1979 ; Cook and Hayward 1983 ; Reed 1991 ; Santagata and
Banta 1996 ; see also Taylor 1988 ). If so, the questions to be
answered are: How many times, when and in which lineages did embryo incubation evolve? How did different
brood-chamber types evolve in cheilostomes and what were
the main trends during their further transformation?
2.4.1 External Membranous Brood Sacs
The simplest brood chambers are external membranous
sacs, although the questions surrounding their origin and
wall composition are still open. Waters ( 1896 [1898] , p. 4,
pl. 1, fi gs. 1–3, 1913 , pl. 64, fi g. 1) discovered them (calling
“ovicells”) in Aetea sica (as A. anguina forma recta ) and A .
anguina , depicting them on top of the dorsal side of the
erect portion in autozooids. In contrast, Robertson ( 1905 , p.
246) recorded a “membranous bag”, situated “on the ventral side” of the zooid “below the operculum but exterior to
the aperture” in A . anguina . She suggested that the curvature of the tubular part of the zooid “afford[s]… protection
to the delicate ooecium and its contents”. In considering the
“great transparency” and position of this brooding structure, Levinsen ( 1909 , p. 93), concluded that “the supposed
ovicellular wall [is] only … a shell membrane surrounding
the egg,” a view accepted by Ström ( 1977 ). Waters ( 1913 )
challenged it, saying that the position of all the brood sacs
he saw was consistent. He referred to Osburn ( 1912 ), who
also depicted the brood sacs at the top of the autozooid,
distal to the operculum in A . anguina . Waters ( 1913 , p. 464)
additionally wrote: “One section shows the zooecial wall
bulging out and the ovum partly in this portion, which is the
commencement of the ovicell.” Although membranous
brood sacs have nothing to do with true ovicells, this observation is in accord with the later suggestion of Cheetham
(personal communication in Cook 1977b ) that this sac
might be an outgrowth of the cystid wall with a coelomic
space inside.
Further researchers have supported both opinions on the
position of these “ooecia” or “ovisacs”. It has been described
as attached to the frontal membrane proximal to the operculum (Marcus 1937 ; Hastings 1943 , pp. 471–472; Gautier
1962 , p. 27; Mawatari 1973b , p. 413) and to the dorsal side
(Marcus 1940 , pp. 103–105; Cook 1968b , p. 137, 1977b ,
1985 ) (reviewed in Prenant and Bobin 1966 and Cook
1968b ). Problematically, all of the above authors have
described the “ovisac” as either proximal or distal in the
same species, Aetea anguina (see also Ryland and Hayward
1977 ; Cook 1985 ). Cook ( 1968b , p. 137) stressed that “the
occurrence of ovisacs either in the dorsal or ventral position
is remarkably consistent in the populations where they are
abundant,” suggesting also that different authors may in
fact have been dealing with different species. For instance,
among more than 100 membranous sacs studied by Cook
( 1968b , fi g. 2D), all were dorsal, though asymmetrical
(dorsal or dorsolateral). Occhipinti Ambrogi ( 1981 )
described these sacs as situated either proximal or distal to
the operculum in A . anguina (also cited in Hayward and
Ryland 1998 ). Both positions are also reported in A . sica
(summarized in Ryland and Hayward 1977 ; Hayward and
Ryland 1998 ; see also Prenant and Bobin 1966 ).
Hastings ( 1943 ) noted that sacs containing an early
embryo were closely applied to the zooidal frontal membrane, whereas those with an advanced embryo were attached
to the membrane by a narrow distal zone that is also evident
in empty sacs (1943, fi g. 57). Similarly, a narrow basal part
of “the membranous ovicelligeous sac” was described and
depicted by Mawatari ( 1973b , p. 414, fi g. 1E, F). Also
Hayward and Ryland ( 1998 , p. 100) wrote that those “ovisacs”
that were situated proximal to the autozooidal orifi ce were at
fi rst appressed to the frontal membrane, but later became free
except for an attachment site proximal to the operculum.
According to Cook ( 1977b , p. 59), the sac is “closely apposed
to the dorsal part of the zooid body wall but attached only in
its distal end.”
Interestingly, Mawatari ( 1973b , p. 414) misinterpreted
Busk ( 1849 , but mistakenly referenced as 1884 ) as having
observed a “membranous ovicelligeous sac” in Aetea , comparing it with “the bag of the pelicans beak”. Busk’s ( 1849 ,
p. 125) text in fact speaks of the membranous frontal wall in
this way, not the brood sac.
2 Cheilostome Brood Chambers: Structure, Formation, Evolution