57
EEN, these observations appear to have been either forgotten
or overlooked (reviewed in Ostrovsky 2008a ; Ostrovsky
et al. 2008 ). Reid ( 1845 , р. 398) was the fi rst to describe the
hypertrophied cellular layer [embryophore] of the distal
wall of the ooecial vesicle that closes the opening of the
brood chamber (ovicell) in the cheilostome Bugula fl abellata.
He wrote that the “membranous partition [ooecial vesicle]
was much thickened, especially at the central part …, and
contained a number of nucleated cells”. The “thickened
wall” of the ooecial vesicle during embryo brooding was
also mentioned by Hincks ( 1861 ), and studied in more detail
by Vigelius ( 1886 ) and Calvet ( 1900 ) who used anatomical
sections. Enlargement of the embryo during incubation was
illustrated or otherwise reported mainly in Bugula and
Bicellariella (Bugulidae) (Reid 1845 ; Hincks 1861 , 1873 ;
Nitsche 1869 ; Vigelius 1886 ; Calvet 1900 ). The implications of their observations were largely not considered further, although Calvet ( 1900 ) noted that a particular cell size
in the wall of the brood sac surrounding the embryo in
Cellaria fi stulosa (Cellariidae) corresponded to a stage in
embryonic development. He nicely illustrated in Bugula
simplex how the epithelium of the ooecial vesicle is not
hypertrophied in an ovicell containing the zygote, whereas
these cells have a columnar shape when a large embryo
occupies the brood chamber. He did not explain this,
however.
Harmer ( 1902 , р. 301) was the fi rst to propose that an
embryo “receives its yolk while in the [brood] sac.” He
compared the relative sizes of the small oviposed oocyte and
the late embryo that fi lls half the zooid cavity in Retifl ustra
schoenaui (Flustridae). Harmer ( 1926 , р. 253–254) later
mentioned a thickening of the “secretory epithelium [of the
brood-sac wall], providing nutriment for the developing
embryo” during embryonic incubation, and noted that the
late embryo occupies two-thirds of the maternal zooid in
this species. He also suggested that the change from brooding in external brood chambers (ovicells) to incubation in
an internal sac “has probably been induced by the supply of
an increased amount of nutrient yolk to the embryo”.
Moreover, Harmer wrote that in the genus Bugula “the
ovum is small when it fi rst passes into the brood-space”,
explaining its increase in size by the nutritive activity of the
ooecial vesicle “which thus acts as a placenta” (p. 203) (see
also Sect. 1.2 ).
Waters ( 1909 , 1912 ) recorded internal brooding in eight
species from the families Watersiporidae, Adeonidae and
Beaniidae. In contrast with Watersipora sp., in which
embryos were described and depicted as enveloped by a “thinwalled [internal brood] sac” (Waters 1909 , pl. 15, fi g. 4, 1912 ,
p. 495), the others were characterized by a “thick-walled
sac”. Judging from Waters’ observations on four adeonid
genera [in which embryos occupied half or even most of the
zooid cavity whereas their eggs were only small to moderate
in size], there is good evidence for EEN. In a subsequent
paper, Waters ( 1913 ) described and depicted hypertrophied
epithelium in an embryo-containing brood sac in Adeonella
lichenoides and Adeonellopsis crosslandi . In Poricellaria
ratoniensis (Poricellariidae), the small egg begins its growth
within the small brood sac, hanging below the zooidal operculum. It then enlarges to such an extent that it fi lls most of
the zooidal cavity, but Waters reached no defi nite conclusion
about this. However, he noted EEN in Catenicella elegans
(Catenicellidae), since he wrote that there are “several fl eshy
bands or tubes by which … material for growth is transferred
to the ovicell” ( 1913 , p. 484).
Embryo enlargement and/or placental analogues in
Bugula stolonifera were described and depicted by Marcus
( 1938a , p. 120) who wrote that while nourishing an embryo
the tall cells of the ooecial vesicle produced an “albuminous
liquid”, i.e. act as a placenta would. His data on the sizes of
oocytes and larvae also point to the existence of EEN in
Celleporella sp. (probably C. carolinensis ; see Ryland 1979
for discussion) (Hippothoidae), Hippopodina feegensis
(Hippopodinidae), and, supporting Waters ( 1913 ), in
Catenicella elegans . In contrast, embryo enlargement was
not detected in congeneric C . contei .
Subsequently Marcus ( 1941b , p. 232) reported viviparity
(intracoelomic embryonic development) in Synnotum
sp. (Epistomiidae). He stated that the embryo “is nourished
by the follicle cells which receive alimentary material from
other parts of the colony and the maternal brown body,
transported by the mesenchymatous tissue- cords”. The late
embryo is 50–60 times larger than the mature ovum before
cleavage, providing strong evidence for EEN.
Embryo enlargement and a “placenta-like system” were
subsequently described and/or illustrated in the brooders
Bugula foliolata , B. neritina , Bicellariella ciliata, Watersipora
cucullata , Celleporella hyalina and Scrupocellaria ferox
(Candidae) (Corrêa 1948 ; Mawatari 1952 ; Woollacott and
Zimmer 1972a , b , 1975 ; Dyrynda and Ryland 1982 ; Dyrynda
and King 1983 ; Hughes 1987 ; Santagata and Banta 1996 ;
Ostrovsky 1998 ; Moosbrugger et al. 2012 ) and viviparous
Epistomia bursaria (Dyrynda 1981 ; Dyrynda and King
1982 ). Embryo enlargement was also recorded in C. carolinensis (Ryland 1979 ), Watersipora arcuata (Zimmer, personal
communication in Reed 1991 ) and Crassimarginatella falcata
(Cook 1985 ).
Additionally, the existence of EEN in Bicellariella ciliata
(Bugulidae) was noted by Ryland ( 1976 ), who, using data of
Nitsche ( 1869 ), compared the size of the small oviposed egg
and the full-grown larva. Dyrynda and King ( 1983 ) also
compared embryo enlargement increase in six matrotrophic
species of Bugula .
Thus, based on published descriptions and illustrations,
EEN has been recorded in 18 genera belonging to 13 families of
Cheilostomata, in the families Flustridae ( Retifl ustra ), Bugulidae
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
EEN, these observations appear to have been either forgotten
or overlooked (reviewed in Ostrovsky 2008a ; Ostrovsky
et al. 2008 ). Reid ( 1845 , р. 398) was the fi rst to describe the
hypertrophied cellular layer [embryophore] of the distal
wall of the ooecial vesicle that closes the opening of the
brood chamber (ovicell) in the cheilostome Bugula fl abellata.
He wrote that the “membranous partition [ooecial vesicle]
was much thickened, especially at the central part …, and
contained a number of nucleated cells”. The “thickened
wall” of the ooecial vesicle during embryo brooding was
also mentioned by Hincks ( 1861 ), and studied in more detail
by Vigelius ( 1886 ) and Calvet ( 1900 ) who used anatomical
sections. Enlargement of the embryo during incubation was
illustrated or otherwise reported mainly in Bugula and
Bicellariella (Bugulidae) (Reid 1845 ; Hincks 1861 , 1873 ;
Nitsche 1869 ; Vigelius 1886 ; Calvet 1900 ). The implications of their observations were largely not considered further, although Calvet ( 1900 ) noted that a particular cell size
in the wall of the brood sac surrounding the embryo in
Cellaria fi stulosa (Cellariidae) corresponded to a stage in
embryonic development. He nicely illustrated in Bugula
simplex how the epithelium of the ooecial vesicle is not
hypertrophied in an ovicell containing the zygote, whereas
these cells have a columnar shape when a large embryo
occupies the brood chamber. He did not explain this,
however.
Harmer ( 1902 , р. 301) was the fi rst to propose that an
embryo “receives its yolk while in the [brood] sac.” He
compared the relative sizes of the small oviposed oocyte and
the late embryo that fi lls half the zooid cavity in Retifl ustra
schoenaui (Flustridae). Harmer ( 1926 , р. 253–254) later
mentioned a thickening of the “secretory epithelium [of the
brood-sac wall], providing nutriment for the developing
embryo” during embryonic incubation, and noted that the
late embryo occupies two-thirds of the maternal zooid in
this species. He also suggested that the change from brooding in external brood chambers (ovicells) to incubation in
an internal sac “has probably been induced by the supply of
an increased amount of nutrient yolk to the embryo”.
Moreover, Harmer wrote that in the genus Bugula “the
ovum is small when it fi rst passes into the brood-space”,
explaining its increase in size by the nutritive activity of the
ooecial vesicle “which thus acts as a placenta” (p. 203) (see
also Sect. 1.2 ).
Waters ( 1909 , 1912 ) recorded internal brooding in eight
species from the families Watersiporidae, Adeonidae and
Beaniidae. In contrast with Watersipora sp., in which
embryos were described and depicted as enveloped by a “thinwalled [internal brood] sac” (Waters 1909 , pl. 15, fi g. 4, 1912 ,
p. 495), the others were characterized by a “thick-walled
sac”. Judging from Waters’ observations on four adeonid
genera [in which embryos occupied half or even most of the
zooid cavity whereas their eggs were only small to moderate
in size], there is good evidence for EEN. In a subsequent
paper, Waters ( 1913 ) described and depicted hypertrophied
epithelium in an embryo-containing brood sac in Adeonella
lichenoides and Adeonellopsis crosslandi . In Poricellaria
ratoniensis (Poricellariidae), the small egg begins its growth
within the small brood sac, hanging below the zooidal operculum. It then enlarges to such an extent that it fi lls most of
the zooidal cavity, but Waters reached no defi nite conclusion
about this. However, he noted EEN in Catenicella elegans
(Catenicellidae), since he wrote that there are “several fl eshy
bands or tubes by which … material for growth is transferred
to the ovicell” ( 1913 , p. 484).
Embryo enlargement and/or placental analogues in
Bugula stolonifera were described and depicted by Marcus
( 1938a , p. 120) who wrote that while nourishing an embryo
the tall cells of the ooecial vesicle produced an “albuminous
liquid”, i.e. act as a placenta would. His data on the sizes of
oocytes and larvae also point to the existence of EEN in
Celleporella sp. (probably C. carolinensis ; see Ryland 1979
for discussion) (Hippothoidae), Hippopodina feegensis
(Hippopodinidae), and, supporting Waters ( 1913 ), in
Catenicella elegans . In contrast, embryo enlargement was
not detected in congeneric C . contei .
Subsequently Marcus ( 1941b , p. 232) reported viviparity
(intracoelomic embryonic development) in Synnotum
sp. (Epistomiidae). He stated that the embryo “is nourished
by the follicle cells which receive alimentary material from
other parts of the colony and the maternal brown body,
transported by the mesenchymatous tissue- cords”. The late
embryo is 50–60 times larger than the mature ovum before
cleavage, providing strong evidence for EEN.
Embryo enlargement and a “placenta-like system” were
subsequently described and/or illustrated in the brooders
Bugula foliolata , B. neritina , Bicellariella ciliata, Watersipora
cucullata , Celleporella hyalina and Scrupocellaria ferox
(Candidae) (Corrêa 1948 ; Mawatari 1952 ; Woollacott and
Zimmer 1972a , b , 1975 ; Dyrynda and Ryland 1982 ; Dyrynda
and King 1983 ; Hughes 1987 ; Santagata and Banta 1996 ;
Ostrovsky 1998 ; Moosbrugger et al. 2012 ) and viviparous
Epistomia bursaria (Dyrynda 1981 ; Dyrynda and King
1982 ). Embryo enlargement was also recorded in C. carolinensis (Ryland 1979 ), Watersipora arcuata (Zimmer, personal
communication in Reed 1991 ) and Crassimarginatella falcata
(Cook 1985 ).
Additionally, the existence of EEN in Bicellariella ciliata
(Bugulidae) was noted by Ryland ( 1976 ), who, using data of
Nitsche ( 1869 ), compared the size of the small oviposed egg
and the full-grown larva. Dyrynda and King ( 1983 ) also
compared embryo enlargement increase in six matrotrophic
species of Bugula .
Thus, based on published descriptions and illustrations,
EEN has been recorded in 18 genera belonging to 13 families of
Cheilostomata, in the families Flustridae ( Retifl ustra ), Bugulidae
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata