59
Interzooidal transport of labeled metabolites via funicular
cords has been demonstrated experimentally in bryozoans
(Best and Thorpe 2002 ), so it may be reasonable to suggest
that nutrient transfer from the maternal zooid to the embryophore is by this pathway, whereas embryophore cells deliver
nutrients to the brood cavity. Transfer of nutrients to the
embryophore via funicular cords is also strongly suggested
by greenish-yellow groups of degenerating cells in
Costaticella solida that appear to be remnants of the brown
body. Similar “granules” were found between and inside the
funicular cords, as well as in intercellular spaces and possibly the cytoplasm of both epithelial and funicular cells of the
embryophore. These data support the suggestion of Ryland
( 1976 ) that the brown body is utilized for the needs of EEN
(see also Dyrynda and King 1983 ). The cytological mechanisms involved in the destruction of the degenerating polypide and transfer of the resulting products have been described
extensively (reviewed by Gordon 1977 ), but the question
remains as to how the (parts of the) collapsed cells of the
brown body are moved to the embryophore, and if phagocytosis is involved in this process. Hageman ( 1983 ) wrote that
some ovulated oocytes were phagocytosed by funicular cells,
and this may be an appropriate mechanism for utilization of
the brown body too.
According to Hughes ( 1987 ), the accumulation of yolk in
the oocyte of Celleporella hyalina at early stages of vitellogenesis may result from activity of the nurse cell, as no
pinocytosis was recorded in the oocyte. Microvilli are developed by the oocyte only at the fi nal stage of its sojourn in the
ovary, when some of its surface becomes exposed to the
coelom. Hughes suggested that reserve nutrients are supplied to the female cell directly from the coelomic fl uid,
whereas the source of these nutrients are probably peritoneal storage cells, which contain numerous granules. In my
opinion, this author considered as storage cells some of the
funicular cells involved in the placental complex. Whatever
the case, I have found nutrient storage cells, fi rst described
by Dyrynda and King ( 1983 ) in Bugula fl abellatа , in fi ve
matrotrophic species ( Pterocella scutella , Costaticella solida , Watersipora subtorquata , Reciprocus regalis and B. fl abellata ). For example, in W . subtorquata , these cells were
found on zooid walls as well as in the zooid cavity at the
sites of fusion of the funicular cords. These large, relatively
intensely staining cells are surrounded by small mesothelial
cells (Fig. 1.14A ) and are often found in groups. Their function remains obscure, but perhaps they are involved in EEN
during polypide recycling.
1.3.6 Fertilization and Its Consequences
Intraovarian fertilization is rather uncommon among invertebrates. Apart from bryozoans, it has been recorded in several
cnidarians (scyphozoans, hydrozoans and anthozoans), two
species of turbellarians (genera Otoplana and Phylosyrtis ),
three species of nemerteans (genera Cephalothrix , Carcinonemertes ), rotifers of the genus Seison , the gastropod Fissurella
nubecula , some nematodes and oligochaetes, three species of
viviparous sea stars (genera Patiriella and Asterina ), the
pogonophore Siboglinum ekmani , kamptozoan Pedicellina
cernua , onychophoran Peripatopsis sedgwicki , ascidian
Botrylloides and doliolid Doliolum denticulatum (Adiyodi
and Adiyodi 1983 , 1989 , 1990 ; Byrne and Cerra 1996 ).
Even rarer is fertilization of early oocytes. It has been
recorded in the ovary in turbellarians of the genus
Otomesostoma , rotifers Asplanchna priodonta and Brachionus calycifl orus and annelids Dinophilus , Saccocirrus and
Histriobdella . Early primary oocytes are also fertilized in
sexual ducts in trematodes and cestodes (Ginetsinskaya and
Dobrovolskij 1978 ; Galaktionov and Dobrovolskij 1987 ).
Some sponges also have early fertilization (Adiyodi and
Adiyodi 1983 , 1989 , 1990 ; Wourms 1987 ).
Intraovarian fertilization appears to be characteristic of
most Bryozoa (except malacostegans, in which fusion of
male and female gametes occurs at or near ovulation)
(Temkin 1996 , reviewed in Ostrovsky 2008b ). In fi gures
given by Vigelius ( 1884b , table 5, fi gs. 69 and 71) and
Hughes ( 1987 , pl. 7a), the mature oocyte is surrounded by a
fertilization envelope while still in the ovary (in Chartella
membranaceotruncata and Celleporella hyalina , correspondingly). In both examples, this envelope can be seen
surrounding the free area of an incompletely ovulated oocyte.
Pergens ( 1889 ) noted that ovulated oocytes in Fenestrulina
malusii are surrounded by a “chorion”, evidently also
meaning the fertilization envelope. Harmer ( 1898 ) found
sperm in the ovary of the cyclostome bryozoan Tubulipora
phalangea and suggested that the paranuclear body that he
observed in the ovarian oocytes of several species of the
same genus may be a male pronucleus. Borg ( 1926 ) found a
sperm head in an ovarian oocyte of the cyclostome Crisiella
producta . In phylactolaemates, sperm have been seen in the
ovaries of Plumatella fungosa and Lophopus crystallinus
(Kraepelin 1892 ; Marcus 1934 ; Brien 1953 ). In L . crystallinus , up to 150 spermatozoids may be contained in the ovary
and up to 18 oocytes may be simultaneously fertilized. The
supposition of Braem ( 1897 ) that fertilization occurs in the
brood sac in P . fungosa is highly doubtful (see Reed 1991 ).
Polyspermy, discovered by Bonnevie ( 1907 ) in malacostegans and later noted in two more instances (Mawatari 1952 ;
Temkin 1994 ), obviously leads to developmental failure.
A synopsis of the arguments for “cross-fertilization vs.
self-fertilization” in bryozoans has been presented in
Sects. 1.1 and 1.2.1 (see also Appendix I). Advocates of
self- fertilization had one thing right – male and female
gametes indeed fuse inside the maternal zooid. The fi rst
proof of early syngamy in Gymnolaemata was provided by
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
Interzooidal transport of labeled metabolites via funicular
cords has been demonstrated experimentally in bryozoans
(Best and Thorpe 2002 ), so it may be reasonable to suggest
that nutrient transfer from the maternal zooid to the embryophore is by this pathway, whereas embryophore cells deliver
nutrients to the brood cavity. Transfer of nutrients to the
embryophore via funicular cords is also strongly suggested
by greenish-yellow groups of degenerating cells in
Costaticella solida that appear to be remnants of the brown
body. Similar “granules” were found between and inside the
funicular cords, as well as in intercellular spaces and possibly the cytoplasm of both epithelial and funicular cells of the
embryophore. These data support the suggestion of Ryland
( 1976 ) that the brown body is utilized for the needs of EEN
(see also Dyrynda and King 1983 ). The cytological mechanisms involved in the destruction of the degenerating polypide and transfer of the resulting products have been described
extensively (reviewed by Gordon 1977 ), but the question
remains as to how the (parts of the) collapsed cells of the
brown body are moved to the embryophore, and if phagocytosis is involved in this process. Hageman ( 1983 ) wrote that
some ovulated oocytes were phagocytosed by funicular cells,
and this may be an appropriate mechanism for utilization of
the brown body too.
According to Hughes ( 1987 ), the accumulation of yolk in
the oocyte of Celleporella hyalina at early stages of vitellogenesis may result from activity of the nurse cell, as no
pinocytosis was recorded in the oocyte. Microvilli are developed by the oocyte only at the fi nal stage of its sojourn in the
ovary, when some of its surface becomes exposed to the
coelom. Hughes suggested that reserve nutrients are supplied to the female cell directly from the coelomic fl uid,
whereas the source of these nutrients are probably peritoneal storage cells, which contain numerous granules. In my
opinion, this author considered as storage cells some of the
funicular cells involved in the placental complex. Whatever
the case, I have found nutrient storage cells, fi rst described
by Dyrynda and King ( 1983 ) in Bugula fl abellatа , in fi ve
matrotrophic species ( Pterocella scutella , Costaticella solida , Watersipora subtorquata , Reciprocus regalis and B. fl abellata ). For example, in W . subtorquata , these cells were
found on zooid walls as well as in the zooid cavity at the
sites of fusion of the funicular cords. These large, relatively
intensely staining cells are surrounded by small mesothelial
cells (Fig. 1.14A ) and are often found in groups. Their function remains obscure, but perhaps they are involved in EEN
during polypide recycling.
1.3.6 Fertilization and Its Consequences
Intraovarian fertilization is rather uncommon among invertebrates. Apart from bryozoans, it has been recorded in several
cnidarians (scyphozoans, hydrozoans and anthozoans), two
species of turbellarians (genera Otoplana and Phylosyrtis ),
three species of nemerteans (genera Cephalothrix , Carcinonemertes ), rotifers of the genus Seison , the gastropod Fissurella
nubecula , some nematodes and oligochaetes, three species of
viviparous sea stars (genera Patiriella and Asterina ), the
pogonophore Siboglinum ekmani , kamptozoan Pedicellina
cernua , onychophoran Peripatopsis sedgwicki , ascidian
Botrylloides and doliolid Doliolum denticulatum (Adiyodi
and Adiyodi 1983 , 1989 , 1990 ; Byrne and Cerra 1996 ).
Even rarer is fertilization of early oocytes. It has been
recorded in the ovary in turbellarians of the genus
Otomesostoma , rotifers Asplanchna priodonta and Brachionus calycifl orus and annelids Dinophilus , Saccocirrus and
Histriobdella . Early primary oocytes are also fertilized in
sexual ducts in trematodes and cestodes (Ginetsinskaya and
Dobrovolskij 1978 ; Galaktionov and Dobrovolskij 1987 ).
Some sponges also have early fertilization (Adiyodi and
Adiyodi 1983 , 1989 , 1990 ; Wourms 1987 ).
Intraovarian fertilization appears to be characteristic of
most Bryozoa (except malacostegans, in which fusion of
male and female gametes occurs at or near ovulation)
(Temkin 1996 , reviewed in Ostrovsky 2008b ). In fi gures
given by Vigelius ( 1884b , table 5, fi gs. 69 and 71) and
Hughes ( 1987 , pl. 7a), the mature oocyte is surrounded by a
fertilization envelope while still in the ovary (in Chartella
membranaceotruncata and Celleporella hyalina , correspondingly). In both examples, this envelope can be seen
surrounding the free area of an incompletely ovulated oocyte.
Pergens ( 1889 ) noted that ovulated oocytes in Fenestrulina
malusii are surrounded by a “chorion”, evidently also
meaning the fertilization envelope. Harmer ( 1898 ) found
sperm in the ovary of the cyclostome bryozoan Tubulipora
phalangea and suggested that the paranuclear body that he
observed in the ovarian oocytes of several species of the
same genus may be a male pronucleus. Borg ( 1926 ) found a
sperm head in an ovarian oocyte of the cyclostome Crisiella
producta . In phylactolaemates, sperm have been seen in the
ovaries of Plumatella fungosa and Lophopus crystallinus
(Kraepelin 1892 ; Marcus 1934 ; Brien 1953 ). In L . crystallinus , up to 150 spermatozoids may be contained in the ovary
and up to 18 oocytes may be simultaneously fertilized. The
supposition of Braem ( 1897 ) that fertilization occurs in the
brood sac in P . fungosa is highly doubtful (see Reed 1991 ).
Polyspermy, discovered by Bonnevie ( 1907 ) in malacostegans and later noted in two more instances (Mawatari 1952 ;
Temkin 1994 ), obviously leads to developmental failure.
A synopsis of the arguments for “cross-fertilization vs.
self-fertilization” in bryozoans has been presented in
Sects. 1.1 and 1.2.1 (see also Appendix I). Advocates of
self- fertilization had one thing right – male and female
gametes indeed fuse inside the maternal zooid. The fi rst
proof of early syngamy in Gymnolaemata was provided by
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata