295
initiales”) in the incipient ovaries. He wrote that all of them
had the same characteristics and were “young ovules” at that
stage (p. 296). In this cell cluster, peripheral cells developed
into the “follicular membrane” [ovarian cells], whereas the
central ones began to grow and accumulate yolk granules,
resulting in mature eggs. However, only some of these cells
develop, whereas others degenerate [presumably nurse
cells]. Calvet thought that growing eggs were nourished at
the expense of those that degenerate.
He believed in the idea of intrazooidal self-fertilization
and stated that he observed it inside the zooid cavity of
Bugula simplex , being preceded by the formation of two
polar bodies expelled from the mature, but unfertilized, egg
surrounded by a thin vitelline membrane. It was suggested
that each regenerating polypide produced a new ovary and
testis in hermaphrodite zooids, and the eggs that were
formed at the expense of the fi rst polypide were further fertilized by the sperm of the testis formed by the second
polypide.
Thus, towards the end of the nineteenth century the following features or conditions of gymnolaemate sexual reproduction were recognized:
• Except for sterile zooids, colonies may consist of either
hermaphrodite and/or gonochoristic autozooids with
simultaneous or non-simultaneous maturation of gametes
in both cases; those thought to be gonochoristic may in fact
be hermaphrodite depending on the time of appearance of
the gonad.
• Germ cells originate at the expense of the mesenchyme
[mesothelium], and the formation of early female cells is
associated with either the zooid wall or the early polypide
bud.
• An ovary is situated on the caecum, funicular strand(s)
(often on that connecting the caecum and the cystid wall),
or cystid wall (also connected to the funiculus), and its
position is variable.
• With one exception ( Farrella repens ), testes (sometimes,
paired) are formed in the proximal part of the zooid on the
cystid wall, often at the site where the funiculus attaches
to the wall.
• The main stages of oogenesis and spermatogenesis are
known. There are clear differences in the amount of yolk
deposited in the eggs of different species.
• There are oviparous and viviparous species among
Gymnolaemata. The former produce numerous eggs,
releasing them through the intertentacular organ or genital pore. The number of eggs in viviparous species is
much smaller, and they are brooded in a variety of types
of incubation chamber.
• Sexual reproduction is often accompanied by polypide
degeneration.
• A thin membrane envelopes ovulated eggs and developing embryos, whether brooded or released.
First Half of the Twentieth Century – More
Results
Schulz ( 1901 ) presented some fi ndings on reproduction in
Einhornia crustulenta (as Membranipora membranacea ),
briefl y describing gametogenesis in this species. Both
male and female gametes mature simultaneously, and the
ovary that is covered by mesodermal epithelium [ovary
wall] develops at the expense of funicular tissue, often
close to the pylorus. Interestingly, Schulz wrote that several ovaries are often formed in one zooid, which is in
accord with the data of Calvet ( 1900 ), who mentioned two
ovaries in one zooid of Bugula simplex (see above).
Spermatogenic tissue is formed partly on funicular strands,
partly on cystid walls. Because of simultaneous zooidal
hermaphroditism, Schulz suggested that self-fertilization
took place in this species. He described an intertentacular
organ, stressing that he could observe it in sexually reproducing colonies only. He rejected the idea that it has an
excretory function (Harmer 1892 ), stating that it was used
exclusively as an oviduct.
Data on the presence and position of gonads are incidentally contained in the works of Harmer ( 1902 , 1915 , 1926 ).
Harmer ( 1902 , p. 301) was the fi rst to write that the embryo
“receives its yolk while in the [brood] sac” in Retifl ustra
schoenaui (as Flustra cribriformis ), and this was infl uenced
by the comparison made between the small oviposited egg
and the large embryo. Harmer ( 1926 , p. 253) described “a
secretory epithelium” in the brood-sac wall, stating that the
embryo towards the end of its development “occupies nearly
two thirds” of the cavity of the fertile zooid in this species.
Comparing reproduction among cheilostomes, he stressed
that “[1] while the eggs which develop into Cyphonautes are
always small, with little or no yolk, and are produced in considerable numbers … [2] the egg which develops in an ovicell is, with few exceptions, single and usually has from the
fi rst a considerable amount of yolk”. He noted as exceptions
the species of Bugula “where [3] the ovum is small when it
fi rst passes into the brood-space. Its increase in size is presumably due to nutriment supplied through the membranous
vesicle, which thus acts as a placenta” (Harmer 1926 , p.
203). Thus, Harmer was actually the fi rst scholar to recognize extraembryonic nutrition and the three major reproductive patterns in Bryozoa.
In the ctenostome Nolella papuensis , Harmer (1915, p.
56) found embryos (surrounded by a thin envelope) immersed
in the zooid cavity and also attached to the zooid wall, and
described them from the viewpoint of Prouho ( 1892 ) as if
they were brooded internally before escaping through a
“hernia- like protrusion”. In the cheilostome genus
Steginoporella (as Steganoporella ) Harmer described
embryos in ovisacs, ovaries on the lateral wall of A-zooids
and sperm in both A- and B-zooids (Harmer 1926 ).
Appendices
initiales”) in the incipient ovaries. He wrote that all of them
had the same characteristics and were “young ovules” at that
stage (p. 296). In this cell cluster, peripheral cells developed
into the “follicular membrane” [ovarian cells], whereas the
central ones began to grow and accumulate yolk granules,
resulting in mature eggs. However, only some of these cells
develop, whereas others degenerate [presumably nurse
cells]. Calvet thought that growing eggs were nourished at
the expense of those that degenerate.
He believed in the idea of intrazooidal self-fertilization
and stated that he observed it inside the zooid cavity of
Bugula simplex , being preceded by the formation of two
polar bodies expelled from the mature, but unfertilized, egg
surrounded by a thin vitelline membrane. It was suggested
that each regenerating polypide produced a new ovary and
testis in hermaphrodite zooids, and the eggs that were
formed at the expense of the fi rst polypide were further fertilized by the sperm of the testis formed by the second
polypide.
Thus, towards the end of the nineteenth century the following features or conditions of gymnolaemate sexual reproduction were recognized:
• Except for sterile zooids, colonies may consist of either
hermaphrodite and/or gonochoristic autozooids with
simultaneous or non-simultaneous maturation of gametes
in both cases; those thought to be gonochoristic may in fact
be hermaphrodite depending on the time of appearance of
the gonad.
• Germ cells originate at the expense of the mesenchyme
[mesothelium], and the formation of early female cells is
associated with either the zooid wall or the early polypide
bud.
• An ovary is situated on the caecum, funicular strand(s)
(often on that connecting the caecum and the cystid wall),
or cystid wall (also connected to the funiculus), and its
position is variable.
• With one exception ( Farrella repens ), testes (sometimes,
paired) are formed in the proximal part of the zooid on the
cystid wall, often at the site where the funiculus attaches
to the wall.
• The main stages of oogenesis and spermatogenesis are
known. There are clear differences in the amount of yolk
deposited in the eggs of different species.
• There are oviparous and viviparous species among
Gymnolaemata. The former produce numerous eggs,
releasing them through the intertentacular organ or genital pore. The number of eggs in viviparous species is
much smaller, and they are brooded in a variety of types
of incubation chamber.
• Sexual reproduction is often accompanied by polypide
degeneration.
• A thin membrane envelopes ovulated eggs and developing embryos, whether brooded or released.
First Half of the Twentieth Century – More
Results
Schulz ( 1901 ) presented some fi ndings on reproduction in
Einhornia crustulenta (as Membranipora membranacea ),
briefl y describing gametogenesis in this species. Both
male and female gametes mature simultaneously, and the
ovary that is covered by mesodermal epithelium [ovary
wall] develops at the expense of funicular tissue, often
close to the pylorus. Interestingly, Schulz wrote that several ovaries are often formed in one zooid, which is in
accord with the data of Calvet ( 1900 ), who mentioned two
ovaries in one zooid of Bugula simplex (see above).
Spermatogenic tissue is formed partly on funicular strands,
partly on cystid walls. Because of simultaneous zooidal
hermaphroditism, Schulz suggested that self-fertilization
took place in this species. He described an intertentacular
organ, stressing that he could observe it in sexually reproducing colonies only. He rejected the idea that it has an
excretory function (Harmer 1892 ), stating that it was used
exclusively as an oviduct.
Data on the presence and position of gonads are incidentally contained in the works of Harmer ( 1902 , 1915 , 1926 ).
Harmer ( 1902 , p. 301) was the fi rst to write that the embryo
“receives its yolk while in the [brood] sac” in Retifl ustra
schoenaui (as Flustra cribriformis ), and this was infl uenced
by the comparison made between the small oviposited egg
and the large embryo. Harmer ( 1926 , p. 253) described “a
secretory epithelium” in the brood-sac wall, stating that the
embryo towards the end of its development “occupies nearly
two thirds” of the cavity of the fertile zooid in this species.
Comparing reproduction among cheilostomes, he stressed
that “[1] while the eggs which develop into Cyphonautes are
always small, with little or no yolk, and are produced in considerable numbers … [2] the egg which develops in an ovicell is, with few exceptions, single and usually has from the
fi rst a considerable amount of yolk”. He noted as exceptions
the species of Bugula “where [3] the ovum is small when it
fi rst passes into the brood-space. Its increase in size is presumably due to nutriment supplied through the membranous
vesicle, which thus acts as a placenta” (Harmer 1926 , p.
203). Thus, Harmer was actually the fi rst scholar to recognize extraembryonic nutrition and the three major reproductive patterns in Bryozoa.
In the ctenostome Nolella papuensis , Harmer (1915, p.
56) found embryos (surrounded by a thin envelope) immersed
in the zooid cavity and also attached to the zooid wall, and
described them from the viewpoint of Prouho ( 1892 ) as if
they were brooded internally before escaping through a
“hernia- like protrusion”. In the cheilostome genus
Steginoporella (as Steganoporella ) Harmer described
embryos in ovisacs, ovaries on the lateral wall of A-zooids
and sperm in both A- and B-zooids (Harmer 1926 ).
Appendices