297
Dendrobeania murrayana (the type species of Dendrobeania
Levinsen, 1909 ) from the genus Bugula on the basis of ovarian structure. In this regard, Waters was in accord with
Vigelius ( 1886 ), who noted a marked difference in the structure of the ovary wall in Bugula and Chartella . Actually, this
distinction refl ected the existence of two different reproductive patterns, involving placental and non-placental brooding associated with micro- and macrolecithal oogenesis
correspondingly, in Cheilostomata, the general appreciation
of which came much later.
Pace ( 1906 ) studied reproduction in the ctenostome
Flustrellidra hispida (as Flustrella ) in detail. He was one of
the fi rst to record gonad activity throughout the different seasons, noting that the simultaneous presence of male and
female gonads in the same zooid is not refl ected in simultaneous maturation. Both male and female germ cells were
reported as originating from the mesenchyme, with the testes
positioned on the body wall and the ovary on the funiculus.
The incipient ovary was stated to originate from a “protoplasmic mass,” with nuclei but no indication of “cell-walls”
(p. 441). Similarly, Owrid and Ryland ( 1991 ) wrote that the
boundaries between young oocytes were occasionally indistinct in the developing ovary in Alcyonidium hirsutum (see
below). These appear later, dividing the “mass” into cells.
Four or fi ve of them differentiate into growing eggs, simultaneously developing in the ovary, whereas the rest develop
into follicle cells. The number of follicle cells increases as
egg maturation proceeds in such a manner that each ripe
“ovum is surrounded by a follicular membrane” (p. 442).
Pace carefully described oocyte growth, with corresponding
changes in its structure, including the fate of the so-called
“yolk nucleus”. Upon egg maturation, the polypide degenerates and up to fi ve oocytes then move to the tentacle sheath
for simultaneous brooding. Similar observations were also
made by Prouho ( 1892 ). In one instance Pace found a “vitelline membrane” [fertilization envelope] and two polar bodies
appearing soon after oviposition, but he could not ascertain
the exact moment of fertilization. During their development,
the embryos increased in size, eventually fi lling the entire
zooidal cavity providing what could be evidence for extraembryonic nutrition.
In contrast with previous authors, Silbermann ( 1906 )
stated that the ovary originates from the ectoderm of the cystid wall in the ctenostome Alcyonidium mytili . Silbermann
followed its development, formation of the follicle and
oocyte growth. As with ovarian development in Flustrellidra
hispida , each large oocyte is enveloped by its own follicle.
Testes are described as being paired, forming on the zooid
wall in the proximal region of the cystid. Hermaphrodite
zooids are rare, however. Moreover, since the author never
saw mature eggs and ripe sperm together [indicative of protogyny?], he concluded that self-fertilisation is impossible in
this case. He described the intertentacular organ in this
species, depicting it sectioned, but Marcus ( 1926a ) stated
that he was mistaken.
Retzius ( 1904 , 1905 , 1906 , 1909 , 1910 ) investigated spermatogenesis and sperm structure in four gymnolaemate species, undertaking one of the most complete and detailed
studies of the time. During the same period the prominent
papers of Bonnevie ( 1906 , 1907 ) were published. Working
on Electra pilosa (as Membranipora ) and Membranipora
membranacea , she revealed that their colonies consist of
male, female and hermaphrodite zooids throughout the
reproductive season. However, all of them are actually protandrous hermaphrodites, possessing either (1) mature sperm
and an early ovary, (2) mature eggs and degenerating sperm
tissue, or (3) sperm and eggs together [probably ripe or
maturing]. Bonnevie suggested that changes in sex proceed
from male to hermaphrodite, and then to the female state in
some zooids, but also that the appearance of the different
gonads may repeatedly alternate during the life span of the
zooid. Both gonads are said to develop from the “parietal
wall of coelom” ( 1907 , p. 567). Spermatogenic tissue develops on the lateral walls. In her study of spermatogenesis,
Bonnevie recorded sperm clusters, spermatozeugmata
(called “spermosyzygien” or “spermozeugmen”), and
described their structure and behaviour in both species. She
noted that spermatozeugmata move independently as a single unit, a possible adaptation for “Polyspermie” – fertilization by several spermatozoids, suggested to occur just after
ovulation. Based on sections, Bonnevie described several
male pronuclei inside the egg, at fi rst positioned close
together, but then later distributed more widely throughout
the cytoplasm and with a spiral shape. She speculated that
clustering of spermatozoids might enhance their locomotory
power, but admitted that this would contradict her own belief
in either intrazooidal or intracolonial self-fertilization.
Judging from her description, she considered polyspermy to
be the rule, ascribing to it a special physiological function.
Additionally, Bonnevie ( 1907 ) studied ovarian structure
and oogenesis of E . pilosa , describing eventual internal
zonation of the ovary with young and mature oocytes having
different shapes and concentrated in different regions
(peripheral and central), and the intermediate stages. She
paid great attention to changes in the nuclear apparatus and
cytoplasmic inclusions of the developing female cells. Based
on nuclear structure, Bonnevie suggested that multiplication
of the cells occurs in the zone with young oocytes. Further
development of the oocyte was said to be accompanied by its
fusion with a “Nährzelle” (“nourishing cell”), “belonging to
the ovarian wall” ( 1907 , p. 585). Fusion was described as a
slow process, with the nucleus of the “nourishing cell” seen
in the oocyte cytoplasm for a long time afterwards.
Subsequent changes in oocyte shape and germinal-vesicle
breakdown were recorded at the beginning of vitellogenesis.
She speculated that nucleoplasm (“cell juice”) is moved
Appendices
Dendrobeania murrayana (the type species of Dendrobeania
Levinsen, 1909 ) from the genus Bugula on the basis of ovarian structure. In this regard, Waters was in accord with
Vigelius ( 1886 ), who noted a marked difference in the structure of the ovary wall in Bugula and Chartella . Actually, this
distinction refl ected the existence of two different reproductive patterns, involving placental and non-placental brooding associated with micro- and macrolecithal oogenesis
correspondingly, in Cheilostomata, the general appreciation
of which came much later.
Pace ( 1906 ) studied reproduction in the ctenostome
Flustrellidra hispida (as Flustrella ) in detail. He was one of
the fi rst to record gonad activity throughout the different seasons, noting that the simultaneous presence of male and
female gonads in the same zooid is not refl ected in simultaneous maturation. Both male and female germ cells were
reported as originating from the mesenchyme, with the testes
positioned on the body wall and the ovary on the funiculus.
The incipient ovary was stated to originate from a “protoplasmic mass,” with nuclei but no indication of “cell-walls”
(p. 441). Similarly, Owrid and Ryland ( 1991 ) wrote that the
boundaries between young oocytes were occasionally indistinct in the developing ovary in Alcyonidium hirsutum (see
below). These appear later, dividing the “mass” into cells.
Four or fi ve of them differentiate into growing eggs, simultaneously developing in the ovary, whereas the rest develop
into follicle cells. The number of follicle cells increases as
egg maturation proceeds in such a manner that each ripe
“ovum is surrounded by a follicular membrane” (p. 442).
Pace carefully described oocyte growth, with corresponding
changes in its structure, including the fate of the so-called
“yolk nucleus”. Upon egg maturation, the polypide degenerates and up to fi ve oocytes then move to the tentacle sheath
for simultaneous brooding. Similar observations were also
made by Prouho ( 1892 ). In one instance Pace found a “vitelline membrane” [fertilization envelope] and two polar bodies
appearing soon after oviposition, but he could not ascertain
the exact moment of fertilization. During their development,
the embryos increased in size, eventually fi lling the entire
zooidal cavity providing what could be evidence for extraembryonic nutrition.
In contrast with previous authors, Silbermann ( 1906 )
stated that the ovary originates from the ectoderm of the cystid wall in the ctenostome Alcyonidium mytili . Silbermann
followed its development, formation of the follicle and
oocyte growth. As with ovarian development in Flustrellidra
hispida , each large oocyte is enveloped by its own follicle.
Testes are described as being paired, forming on the zooid
wall in the proximal region of the cystid. Hermaphrodite
zooids are rare, however. Moreover, since the author never
saw mature eggs and ripe sperm together [indicative of protogyny?], he concluded that self-fertilisation is impossible in
this case. He described the intertentacular organ in this
species, depicting it sectioned, but Marcus ( 1926a ) stated
that he was mistaken.
Retzius ( 1904 , 1905 , 1906 , 1909 , 1910 ) investigated spermatogenesis and sperm structure in four gymnolaemate species, undertaking one of the most complete and detailed
studies of the time. During the same period the prominent
papers of Bonnevie ( 1906 , 1907 ) were published. Working
on Electra pilosa (as Membranipora ) and Membranipora
membranacea , she revealed that their colonies consist of
male, female and hermaphrodite zooids throughout the
reproductive season. However, all of them are actually protandrous hermaphrodites, possessing either (1) mature sperm
and an early ovary, (2) mature eggs and degenerating sperm
tissue, or (3) sperm and eggs together [probably ripe or
maturing]. Bonnevie suggested that changes in sex proceed
from male to hermaphrodite, and then to the female state in
some zooids, but also that the appearance of the different
gonads may repeatedly alternate during the life span of the
zooid. Both gonads are said to develop from the “parietal
wall of coelom” ( 1907 , p. 567). Spermatogenic tissue develops on the lateral walls. In her study of spermatogenesis,
Bonnevie recorded sperm clusters, spermatozeugmata
(called “spermosyzygien” or “spermozeugmen”), and
described their structure and behaviour in both species. She
noted that spermatozeugmata move independently as a single unit, a possible adaptation for “Polyspermie” – fertilization by several spermatozoids, suggested to occur just after
ovulation. Based on sections, Bonnevie described several
male pronuclei inside the egg, at fi rst positioned close
together, but then later distributed more widely throughout
the cytoplasm and with a spiral shape. She speculated that
clustering of spermatozoids might enhance their locomotory
power, but admitted that this would contradict her own belief
in either intrazooidal or intracolonial self-fertilization.
Judging from her description, she considered polyspermy to
be the rule, ascribing to it a special physiological function.
Additionally, Bonnevie ( 1907 ) studied ovarian structure
and oogenesis of E . pilosa , describing eventual internal
zonation of the ovary with young and mature oocytes having
different shapes and concentrated in different regions
(peripheral and central), and the intermediate stages. She
paid great attention to changes in the nuclear apparatus and
cytoplasmic inclusions of the developing female cells. Based
on nuclear structure, Bonnevie suggested that multiplication
of the cells occurs in the zone with young oocytes. Further
development of the oocyte was said to be accompanied by its
fusion with a “Nährzelle” (“nourishing cell”), “belonging to
the ovarian wall” ( 1907 , p. 585). Fusion was described as a
slow process, with the nucleus of the “nourishing cell” seen
in the oocyte cytoplasm for a long time afterwards.
Subsequent changes in oocyte shape and germinal-vesicle
breakdown were recorded at the beginning of vitellogenesis.
She speculated that nucleoplasm (“cell juice”) is moved
Appendices