300
timing of egg liberation. A second generation of oocytes
often appears in the zooids bearing embryos. Larvae escape
from the brood sac presumably through the rupture of its
wall. It is possible that these “brood-sacs” are fertilization
envelopes that stick to the operculum (see Ström 1977 ).
Brief reviews of bryozoan sexual reproduction were published by Marcus ( 1926b , 1940 ). The following “Brazilian”
papers of this author are an outstanding synthesis of data
from the literature and his own results on taxonomy, morphology and reproductive biology, written in Portuguese
with an English summary (Marcus 1937 , 1938a , 1939 ,
1941a , b , 1942 ). Marcus described zooidal polymorphism
and the sequential appearance of male and female zooids in
two hippothoid cheilostomes (as Hippothoa hyalina ), calling
them protandrous, and stressing that self-fertilization is
impossible when male and female sex cells mature at different times ( 1937 , 1938a ). He did not see any parietal muscles
[eventually discovered by Ostrovsky ( 1998 )] associated with
the ascus in female zooids and was sure that the
2–3- tentaculate rudimentary polypide could not protrude in
this species. On the other hand, he did witness protrusions of
6-tentaculate rudimentary male polypides, implicating them
in sperm release. Spermatozoids were discovered in the coeloms of all three zooid types [sterile autozooids and sexual
polymorphs], leading Marcus to suggest that sperm go “in
search of the eggs” ( 1938a , pp. 77, 119), perhaps migrating
within a colony via pore-chambers. It is logical to suggest
that alien sperm are accepted fi rst by the expanded lophophores of autozooids, in which Marcus reported the coelomopore, but this idea seems absent from his text. He
discovered spermatozeugmata in the cheilostome Bifl ustra
savartii (as Acanthodesia ), but showed (from sections) that
fertilization is monospermic. In this and 16 other gymnolaemate species, Marcus noted the presence of either the supraneural pore (“póro supraneural”, p. 86) or intertentacular
organ. He also gave a list of species and papers in which
similar observations were described.
Among his most interesting and important discoveries
was precocious intraovarian fertilization [syngamy] in two
ctenostomes – Alcyonidium sp. (as A. mamillatum ) and
Nolella stipata (as N . gigantea ) – and a number of cheilostomes. As mentioned above, previous authors believed that
fertilization occurs after ovulation or later. Marcus ( 1938a )
stated that this fi nding explains how the timing of gonadal
maturation is connected with fertilization. He wrote that a
fully grown ovary in zooids without testes may already contain [alien] sperm, suggesting cross-fertilization. However,
distinct protandry [in hermaphrodite zooids] “by no means
indicates that there must be reciprocal fertilization” since
even early oocytes can be fertilized in the same zooid by its
own sperm (p. 120). From this fi nding it also follows that
simultaneous maturation of the gametes in a zooid or colony
cannot be regarded as evidence for self-fertilization if the
fusion of the male and female cells is precocious [i.e. occurs
before sperm maturation]. Marcus noted that syngamy happens “in the beginning of their [oocytes] second growing
period” (p. 119). In fact, the diameter of fertilized oocytes
measured ca. 20.0 μm in Celleporina costazii (as Siniopelta )
and Rhynchozoon phrynoglossum , prior to vitellogenesis. In
the ctenostomes Alcyonidium sp. and N . stipata , sperm was
found in oocytes “which are still growing” (p. 81). Four of
Marcus’s fi gures ( 1938a , pl. 3, fi g. 8B, pl. 21, fi gs 58–60) of
cheilostome ovaries show previtellogenic or early vitellogenic oocytes or oocyte doublets with a male pronucleus in
the cytoplasm. Sperm heads were also found between ovarian
cells. Mature oocytes were described as being not completely
covered with follicular cells, but partially exposed to the
zooidal coelom. Oocytes were described as differing in
the amount of yolk, “scarce in Bugula , considerable in
Hippopodina ” [oligo- and macrolecithal, correspondingly]
(p. 121). Maturation divisions [Marcus obviously meant the
breakdown of the nuclear membrane] began in the ovary or
immediately following ovulation. In contrast with all the
other oviparous species studied, Arbocuspis bellula (as
Electra ) “shows only one mature … egg”, which is, however,
“bigger than in viviparous species” (pp. 88–89, 120). It is not
clear if A. bellula actually belongs to malacostegans since it
could be an internal brooder. Confi rming the data of Prouho
( 1892 ), Marcus found internally brooded embryos on the
zooid wall in the ctenostomes Nolella dilatata and N . alta
(reviewed in Ström 1977 ).
Marcus clearly understood the role of the hypertrophied
epithelium in the ooecial vesicle in cheilostomes. He recognized the presence of extraembryonic nutrition in Bugula
avicularia , comparing this species with non-placental cheilostome brooders and noting a similar fi nding of Waters
( 1913 ) in the cheilostome Catenicella elegans (as
Vittaticella ). He noted that the placenta develops after the
beginning of cleavage and is reduced after larval release, and
that the hypertrophied cells of the embryophore supply the
embryo with a presumed “albuminous liquid” ( 1938a , p. 120).
Marcus also mentioned enlargement of embryophore cells,
previously recorded by Vigelius ( 1886 ) and Calvet ( 1900 ).
His data on the sizes of mature eggs, early embryos and incubated larvae showed the possibility of extraembryonic nutrition in Celleporella sp. (as Hippothoa hyalina ), Hippopodina
feegensis and Catenicella elegans . However, Marcus stated
that there is no such nutrition in Catenicella contei , again
comparing the size of the egg and the embryo (discussed also
in Ryland 1976 ). He suggested that synchronized growth of
both the next egg in the ovary and the nourished embryo in
the ovicell is regulated hormonally. Studying embryogenesis
of Bugula species, Marcus recorded the formation of two
polar bodies that remain within the fertilization envelope.
Marcus ( 1941a ) described the reproductive biology of
Thalamoporella evelinae . This species was described as
Appendices
timing of egg liberation. A second generation of oocytes
often appears in the zooids bearing embryos. Larvae escape
from the brood sac presumably through the rupture of its
wall. It is possible that these “brood-sacs” are fertilization
envelopes that stick to the operculum (see Ström 1977 ).
Brief reviews of bryozoan sexual reproduction were published by Marcus ( 1926b , 1940 ). The following “Brazilian”
papers of this author are an outstanding synthesis of data
from the literature and his own results on taxonomy, morphology and reproductive biology, written in Portuguese
with an English summary (Marcus 1937 , 1938a , 1939 ,
1941a , b , 1942 ). Marcus described zooidal polymorphism
and the sequential appearance of male and female zooids in
two hippothoid cheilostomes (as Hippothoa hyalina ), calling
them protandrous, and stressing that self-fertilization is
impossible when male and female sex cells mature at different times ( 1937 , 1938a ). He did not see any parietal muscles
[eventually discovered by Ostrovsky ( 1998 )] associated with
the ascus in female zooids and was sure that the
2–3- tentaculate rudimentary polypide could not protrude in
this species. On the other hand, he did witness protrusions of
6-tentaculate rudimentary male polypides, implicating them
in sperm release. Spermatozoids were discovered in the coeloms of all three zooid types [sterile autozooids and sexual
polymorphs], leading Marcus to suggest that sperm go “in
search of the eggs” ( 1938a , pp. 77, 119), perhaps migrating
within a colony via pore-chambers. It is logical to suggest
that alien sperm are accepted fi rst by the expanded lophophores of autozooids, in which Marcus reported the coelomopore, but this idea seems absent from his text. He
discovered spermatozeugmata in the cheilostome Bifl ustra
savartii (as Acanthodesia ), but showed (from sections) that
fertilization is monospermic. In this and 16 other gymnolaemate species, Marcus noted the presence of either the supraneural pore (“póro supraneural”, p. 86) or intertentacular
organ. He also gave a list of species and papers in which
similar observations were described.
Among his most interesting and important discoveries
was precocious intraovarian fertilization [syngamy] in two
ctenostomes – Alcyonidium sp. (as A. mamillatum ) and
Nolella stipata (as N . gigantea ) – and a number of cheilostomes. As mentioned above, previous authors believed that
fertilization occurs after ovulation or later. Marcus ( 1938a )
stated that this fi nding explains how the timing of gonadal
maturation is connected with fertilization. He wrote that a
fully grown ovary in zooids without testes may already contain [alien] sperm, suggesting cross-fertilization. However,
distinct protandry [in hermaphrodite zooids] “by no means
indicates that there must be reciprocal fertilization” since
even early oocytes can be fertilized in the same zooid by its
own sperm (p. 120). From this fi nding it also follows that
simultaneous maturation of the gametes in a zooid or colony
cannot be regarded as evidence for self-fertilization if the
fusion of the male and female cells is precocious [i.e. occurs
before sperm maturation]. Marcus noted that syngamy happens “in the beginning of their [oocytes] second growing
period” (p. 119). In fact, the diameter of fertilized oocytes
measured ca. 20.0 μm in Celleporina costazii (as Siniopelta )
and Rhynchozoon phrynoglossum , prior to vitellogenesis. In
the ctenostomes Alcyonidium sp. and N . stipata , sperm was
found in oocytes “which are still growing” (p. 81). Four of
Marcus’s fi gures ( 1938a , pl. 3, fi g. 8B, pl. 21, fi gs 58–60) of
cheilostome ovaries show previtellogenic or early vitellogenic oocytes or oocyte doublets with a male pronucleus in
the cytoplasm. Sperm heads were also found between ovarian
cells. Mature oocytes were described as being not completely
covered with follicular cells, but partially exposed to the
zooidal coelom. Oocytes were described as differing in
the amount of yolk, “scarce in Bugula , considerable in
Hippopodina ” [oligo- and macrolecithal, correspondingly]
(p. 121). Maturation divisions [Marcus obviously meant the
breakdown of the nuclear membrane] began in the ovary or
immediately following ovulation. In contrast with all the
other oviparous species studied, Arbocuspis bellula (as
Electra ) “shows only one mature … egg”, which is, however,
“bigger than in viviparous species” (pp. 88–89, 120). It is not
clear if A. bellula actually belongs to malacostegans since it
could be an internal brooder. Confi rming the data of Prouho
( 1892 ), Marcus found internally brooded embryos on the
zooid wall in the ctenostomes Nolella dilatata and N . alta
(reviewed in Ström 1977 ).
Marcus clearly understood the role of the hypertrophied
epithelium in the ooecial vesicle in cheilostomes. He recognized the presence of extraembryonic nutrition in Bugula
avicularia , comparing this species with non-placental cheilostome brooders and noting a similar fi nding of Waters
( 1913 ) in the cheilostome Catenicella elegans (as
Vittaticella ). He noted that the placenta develops after the
beginning of cleavage and is reduced after larval release, and
that the hypertrophied cells of the embryophore supply the
embryo with a presumed “albuminous liquid” ( 1938a , p. 120).
Marcus also mentioned enlargement of embryophore cells,
previously recorded by Vigelius ( 1886 ) and Calvet ( 1900 ).
His data on the sizes of mature eggs, early embryos and incubated larvae showed the possibility of extraembryonic nutrition in Celleporella sp. (as Hippothoa hyalina ), Hippopodina
feegensis and Catenicella elegans . However, Marcus stated
that there is no such nutrition in Catenicella contei , again
comparing the size of the egg and the embryo (discussed also
in Ryland 1976 ). He suggested that synchronized growth of
both the next egg in the ovary and the nourished embryo in
the ovicell is regulated hormonally. Studying embryogenesis
of Bugula species, Marcus recorded the formation of two
polar bodies that remain within the fertilization envelope.
Marcus ( 1941a ) described the reproductive biology of
Thalamoporella evelinae . This species was described as
Appendices