4
gymnolaemates and stenolaemates studied, sperm can be
released via the terminal pores in all tentacles of the feeding
apparatus (Bullivant 1967 ; Silén 1972 ; reviewed in Ostrovsky
and Porter 2011 ). After a free-swimming period, sperm
adhere to the tentacles of a recipient lophophore and actively
migrate towards the intertentacular organ (or coelomopore)
through which oocytes are released. In one species sperm
were observed inside an intertentacular organ.
Several studies devoted to spermatogenesis and sperm
ultrastructure in bryozoans were published by Franzén
( 1956 , 1970 , 1976 , 1977 , 1981 , 1983 , 1987а , b ), who
ascertained that male gametes in Bryozoa are structurally
modifi ed in comparison with sperm of animals with external
fertilization.
Transmission-electron-microscopic (TEM) studies made
by Woollacott and Zimmer ( 1972a , 1975 ) revealed ultrastructural features of extraembryonic nutrition in the cheilostome Bugula neritina . Subsequently, detailed studies of
bryozoan reproduction, most of them using TEM, have been
undertaken by several authors including Nielsen ( 1981 ),
Hageman ( 1983 ), Hughes ( 1987 ) and Dyrynda with coauthors (Dyrynda 1981 ; Dyrynda and Ryland 1982 ; Dyrynda
and King 1982 , 1983 ). Extensive experimental studies by
Hughes and colleagues, using the cheilostome Celleporella
hyalina as a model species, have contributed hugely to
modern understanding of oogenesis and fertilization in
bryozoans (Hunter and Hughes 1993 , 1995 ; Hoare et al. 1999 ;
Manríquez et al. 2001 ; Hughes et al. 2002a , b ). Noteworthy,
although the brilliant research of Temkin ( 1994 , 1996 ) has
demonstrated that internal fertilization, whether intracoelomic
or intraovarian, is obligatory in gymnolaemates, confusing
ideas about self-fertilization (Smith et al. 2003 ) and external
fertilization (Schmidt-Rhaesa 2007 ) continue to surface.
Reed ( 1991 ) summarized previous studies and his own
fi ndings on bryozoan sexual reproduction in an exhaustive
review that was the most complete source of information
since the classic volume by Hyman ( 1959 ). Later analyses of
reproductive patterns in cheilostome bryozoans (Ostrovsky
2009 , 2013 ; Ostrovsky et al. 2009a ; Moosbrugger et al.
2012 ) and the history of research on gymnolaemate reproduction have been published by the present author and coauthors (Ostrovsky 2008a , b ; Ostrovsky et al. 2008 ). All
these summaries show that, in spite of the long history of
studies, our understanding of sexual reproduction in Bryozoa
is still very incomplete. The abundance of bryozoans in
marine bottom communities, their dramatic evolutionary history and extensive paleontological record, as well as their
rich taxonomic and morphological diversity are in poignant
disharmony with the scarcity of information on their reproduction. This monograph aims to close the gap.
In the following sections, the range of variants in the sexual
structure of cheilostome colonies is described, including the
position of the gonads and zooidal sexual polymorphism.
Five reproductive patterns are recognized and their main
attributes (oogenesis, fertilization, oviposition/gamete
release and embryonic incubation) are described in detail,
together with associated structures. Original data are
compared with those in the literature and hypotheses on the
evolution of the various aspects of bryozoan reproduction are
considered. Patterns of sexual reproduction in Ctenostomata
are analysed in Chap. 3 .
1.2
Reproductive Patterns of Bryozoa
In bryozoans, totipotent cells in the cystid wall may differentiate either as somatic cells to produce a new zooid or regenerate a polypide, or as primordial germ cells (PGC) to initiate
sexual reproduction (Reed 1991 ). Thus, there is epigenetic
specifi cation of the sex-cell lineage in this phylum (Extavour
and Akam 2003 ; Dondua 2005 ). Spermatogonia typically
develop within the cystid mesothelium that lines the main
body cavity, while oogonia usually appear in the mesothelial
layer of the polypide bud. Gonads generally lack gonoducts,
although some accessory structures (e.g. ciliary funnel) are
developed in some species. Gametes are released through
the coelomopores. Though bryozoans are hermaphrodites,
cross-fertilization is the norm, although self-fertilization has
been encountered in some experiments (Hughes et al. 2002b ;
Johnson 2010 ; Hughes and Wright, in press ). Release of
sperm is through the terminal tentacle pores. Fertilization
occurs either within the ovary or in the zooidal coelom at
or near ovulation. Fertilized eggs are evacuated via the
intertentacular organ or supraneural coelomopore in
Gymnolaemata; whether such coelomopores are present
in Stenolaemata is unknown. Phylactolaemates possess a
vestibular pore through which release of statoblasts has been
observed (reviewed in Ostrovsky and Porter 2011 ).
Organization of the ovary and patterns of oogenesis vary
throughout the phylum depending upon the particular strategy of sexual reproduction and its consequences for larval
nutrition. As mentioned above, Calvet ( 1900 ) divided bryozoans into oviparous and viviparous types, showing the striking difference in the number of eggs contained in their
ovaries and stressing the presence or absence of embryo
incubation. Harmer ( 1926 ) was the fi rst to recognize the
three major reproductive patterns, distinguished thus: (1) in
Cheilostomata, oocytes that transform into planktotrophic
larvae are always small, contain little yolk and form in large
numbers; (2) in brooding species, on the other hand, a single
egg with a considerable nutrient reserve is transported to the
ovicell; (3) Bugula species are, according to Harmer, an
exception: a small oocyte transferred to the brood chamber
increases in size “presumably due to nutriment supplied
through the membranous vesicle, which thus acts as a placenta” (Harmer 1926 , p. 203) (see also Appendix I).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
gymnolaemates and stenolaemates studied, sperm can be
released via the terminal pores in all tentacles of the feeding
apparatus (Bullivant 1967 ; Silén 1972 ; reviewed in Ostrovsky
and Porter 2011 ). After a free-swimming period, sperm
adhere to the tentacles of a recipient lophophore and actively
migrate towards the intertentacular organ (or coelomopore)
through which oocytes are released. In one species sperm
were observed inside an intertentacular organ.
Several studies devoted to spermatogenesis and sperm
ultrastructure in bryozoans were published by Franzén
( 1956 , 1970 , 1976 , 1977 , 1981 , 1983 , 1987а , b ), who
ascertained that male gametes in Bryozoa are structurally
modifi ed in comparison with sperm of animals with external
fertilization.
Transmission-electron-microscopic (TEM) studies made
by Woollacott and Zimmer ( 1972a , 1975 ) revealed ultrastructural features of extraembryonic nutrition in the cheilostome Bugula neritina . Subsequently, detailed studies of
bryozoan reproduction, most of them using TEM, have been
undertaken by several authors including Nielsen ( 1981 ),
Hageman ( 1983 ), Hughes ( 1987 ) and Dyrynda with coauthors (Dyrynda 1981 ; Dyrynda and Ryland 1982 ; Dyrynda
and King 1982 , 1983 ). Extensive experimental studies by
Hughes and colleagues, using the cheilostome Celleporella
hyalina as a model species, have contributed hugely to
modern understanding of oogenesis and fertilization in
bryozoans (Hunter and Hughes 1993 , 1995 ; Hoare et al. 1999 ;
Manríquez et al. 2001 ; Hughes et al. 2002a , b ). Noteworthy,
although the brilliant research of Temkin ( 1994 , 1996 ) has
demonstrated that internal fertilization, whether intracoelomic
or intraovarian, is obligatory in gymnolaemates, confusing
ideas about self-fertilization (Smith et al. 2003 ) and external
fertilization (Schmidt-Rhaesa 2007 ) continue to surface.
Reed ( 1991 ) summarized previous studies and his own
fi ndings on bryozoan sexual reproduction in an exhaustive
review that was the most complete source of information
since the classic volume by Hyman ( 1959 ). Later analyses of
reproductive patterns in cheilostome bryozoans (Ostrovsky
2009 , 2013 ; Ostrovsky et al. 2009a ; Moosbrugger et al.
2012 ) and the history of research on gymnolaemate reproduction have been published by the present author and coauthors (Ostrovsky 2008a , b ; Ostrovsky et al. 2008 ). All
these summaries show that, in spite of the long history of
studies, our understanding of sexual reproduction in Bryozoa
is still very incomplete. The abundance of bryozoans in
marine bottom communities, their dramatic evolutionary history and extensive paleontological record, as well as their
rich taxonomic and morphological diversity are in poignant
disharmony with the scarcity of information on their reproduction. This monograph aims to close the gap.
In the following sections, the range of variants in the sexual
structure of cheilostome colonies is described, including the
position of the gonads and zooidal sexual polymorphism.
Five reproductive patterns are recognized and their main
attributes (oogenesis, fertilization, oviposition/gamete
release and embryonic incubation) are described in detail,
together with associated structures. Original data are
compared with those in the literature and hypotheses on the
evolution of the various aspects of bryozoan reproduction are
considered. Patterns of sexual reproduction in Ctenostomata
are analysed in Chap. 3 .
1.2
Reproductive Patterns of Bryozoa
In bryozoans, totipotent cells in the cystid wall may differentiate either as somatic cells to produce a new zooid or regenerate a polypide, or as primordial germ cells (PGC) to initiate
sexual reproduction (Reed 1991 ). Thus, there is epigenetic
specifi cation of the sex-cell lineage in this phylum (Extavour
and Akam 2003 ; Dondua 2005 ). Spermatogonia typically
develop within the cystid mesothelium that lines the main
body cavity, while oogonia usually appear in the mesothelial
layer of the polypide bud. Gonads generally lack gonoducts,
although some accessory structures (e.g. ciliary funnel) are
developed in some species. Gametes are released through
the coelomopores. Though bryozoans are hermaphrodites,
cross-fertilization is the norm, although self-fertilization has
been encountered in some experiments (Hughes et al. 2002b ;
Johnson 2010 ; Hughes and Wright, in press ). Release of
sperm is through the terminal tentacle pores. Fertilization
occurs either within the ovary or in the zooidal coelom at
or near ovulation. Fertilized eggs are evacuated via the
intertentacular organ or supraneural coelomopore in
Gymnolaemata; whether such coelomopores are present
in Stenolaemata is unknown. Phylactolaemates possess a
vestibular pore through which release of statoblasts has been
observed (reviewed in Ostrovsky and Porter 2011 ).
Organization of the ovary and patterns of oogenesis vary
throughout the phylum depending upon the particular strategy of sexual reproduction and its consequences for larval
nutrition. As mentioned above, Calvet ( 1900 ) divided bryozoans into oviparous and viviparous types, showing the striking difference in the number of eggs contained in their
ovaries and stressing the presence or absence of embryo
incubation. Harmer ( 1926 ) was the fi rst to recognize the
three major reproductive patterns, distinguished thus: (1) in
Cheilostomata, oocytes that transform into planktotrophic
larvae are always small, contain little yolk and form in large
numbers; (2) in brooding species, on the other hand, a single
egg with a considerable nutrient reserve is transported to the
ovicell; (3) Bugula species are, according to Harmer, an
exception: a small oocyte transferred to the brood chamber
increases in size “presumably due to nutriment supplied
through the membranous vesicle, which thus acts as a placenta” (Harmer 1926 , p. 203) (see also Appendix I).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis