12
between neighbouring colonies (Silén 1966 ). Zimmer
(personal communication in Reed 1991 ) reported similar
fi ndings in Membranipora membranacea . I suggest that
hormonal regulation via an extensive network of funicular
cords plays a vital role in ensuring different levels of colonial
integration and synchronization of reproductive activity
(see also Shunatova and Ostrovsky 2002 ).
With respect to the evolution of colonial sexual structure,
the most advanced expression of zooidal transformation
appears to be morphologically different, sexually polymorphic zooids (see Sects. 1.3.8 and 3.3 ). The question of what
came fi rst, zooidal hermaphroditism or gonochorism,
remains open. Dyrynda and Ryland ( 1982 ) suggested that
gonochoristic zooids could have evolved as a result of
suppression or prolonged delay in the development of one
gonad in the course of the development of the other. If so, the
initial variant in colonial sexual structure would have been a
combination of sterile and hermaphrodite zooids, which is
the commonest mode of expression. This idea accords with
the hypotheses that hermaphroditism is the ancestral mode in
bilaterian animals (Balsamo 1992 ; Schmidt-Rhaesa 2007 )
and that the evolution of hermaphroditism is connected with
a sedentary way of life (Ghiselin 1969 , 1987 ), in which the
likelihood of gamete encounter is reduced in fi xed, spatially
separated colonies. In extreme cases, self-fertilization can be
resorted to (see below). On the other hand, Hughes et al.
( 2002a ) asked why hermaphroditism should be retained in
bryozoans if cross-fertilization is the rule. In further consideration of the potential challenge of achieving fertilization in
sedentary organisms, let me nevertheless note that, in a population of hermaphrodites, all individuals can reproduce
whereas only half can produce offspring in gonochoristic
populations. Moreover, hermaphroditism makes it possible
for a colony to manipulate resources, channelling them for
the production of either male or female gametes depending
on circumstances and thus increasing the probability of fertilization and the effi ciency of larval production (see also
Hughes et al. 2002a ).
1.2.1.1 Hermaphroditism and Cross-Fertilization
The co-occurrence of mature eggs and sperm in hermaphrodite zooids is common in gymnolaemates (Fig. 1. 34C ). It is
therefore not surprising that notions of intrazooidal selffertilization survived in the scientifi c literature until the
beginning of the twenty-fi rst century (Smith et al. 2003 ;
reviewed in Ostrovsky 2008b ; see also Sect. 1.3.6 and
Appendix I). Self-fertilization was assumed by Nordmann
( 1839 ), the fi rst to unambiguously describe sperm in
Bryozoa, and by van Beneden ( 1844a ) (see Sect. 1.1 ). The
former author, who studied Tendra zostericola , wrote that
spermatozoids entered the “female” zooids from “males” via
the opening in their base [supposedly, in the transverse wall],
thus implying the existence of intracolonial self-fertilization.
Van Beneden ( 1844a ) documented the co-occurrence of ripe
eggs and sperm in zooids of the ctenostome Farrella repens ,
and likewise assumed intrazooidal self-fertilization. Calvet
( 1900 ) even stated that he observed self-fertilization take
place in the zooid cavity in Bugula simplex .
As mentioned above, the fi rst researcher to dispute this
general opinion and to argue that cross-fertilization occurred
in some species, ctenostome as well as cheilostome, was
Joliet ( 1877 ). The existence of protandrous zooidal hermaphroditism and zooidal gonochorism, the massive production of spermatozoids, and their release and capability of
swimming actively in the surrounding water led him to
believe that cross-fertilization was the rule. This view was
strongly supported by the observations of Vigelius ( 1884b ),
who was one of the fi rst to describe the dynamics of sexual
changes in bryozoan colonies. Vigelius thought that sperm
release was possible through the zooidal aperture only after
polypide degeneration and destruction of the body wall.
Fertilization itself was supposed to occur externally,
inside the ovicell in brooding cheilostomes. However, the
co- occurrence of male and female gametes in the same
zooid forced him to admit the possibility of intrazooidal
self- fertilization in Bugula calathus (see Vigelius 1886 ).
Notwithstanding, neither Joliet nor Vigelius dwelt upon the
question of whether fertilization was intra- or intercolonial.
In this regard it should be noted that, since bryozoan populations consist of colonies of different age at different stages of
the sexual cycle, those that have only male or only female
gonads at the beginning of reproduction may participate only
in intercolonial cross-fertilization (see Ostrovsky 1998 ).
The discovery of precocious insemination (Marcus
1938a ) devalued the idea about the different timing of gonad
maturation in hermaphrodite zooids as an argument in favour
of cross-fertilization; i.e. if early oocytes can be fertilized in
the ovary, then the prior maturation of sperm in anticipation
of this event is clearly not an obstacle to intrazooidal selffertilization (see also Sect. 1.3.6 ).
The observations of Silén ( 1966 , 1972 ), Bullivant ( 1967 )
and Temkin ( 1994 ) on sperm release via the terminal pores
of the tentacles constituted direct evidence in favour of crossfertilization, as did data on the frequencies of allele distribution in natural populations (Schopf 1977 ; Thorpe et al.
1978a , b ; Thorpe and Beardmore 1981 ; see also Hoare et al.
1999 ). Cross-fertilization is also promoted by the relatively
long life of sperm (Manríquez et al. 2001 ), high effi ciency of
sperm capture by feeding lophophores (Temkin 1994 , 1996 ;
Pemberton et al. 2003 ), ability to store sperm by immature
colonies (Hughes et al. 2002a ) and the usually high population densities of the colonies (see also Hoare and Hughes
2001 ; Bishop and Pemberton 2006 and references therein).
Moreover, experiments with isolated colonies of Celleporella
hyalina showed that intracolonial self-fertilization in most
cases resulted in abortion of embryos, reduced larval fi tness
and low larval numbers (Cancino et al. 1991 ; Hunter and
Hughes 1993 , 1995 ; Hoare and Hughes 2001 ; Hughes et al.
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
between neighbouring colonies (Silén 1966 ). Zimmer
(personal communication in Reed 1991 ) reported similar
fi ndings in Membranipora membranacea . I suggest that
hormonal regulation via an extensive network of funicular
cords plays a vital role in ensuring different levels of colonial
integration and synchronization of reproductive activity
(see also Shunatova and Ostrovsky 2002 ).
With respect to the evolution of colonial sexual structure,
the most advanced expression of zooidal transformation
appears to be morphologically different, sexually polymorphic zooids (see Sects. 1.3.8 and 3.3 ). The question of what
came fi rst, zooidal hermaphroditism or gonochorism,
remains open. Dyrynda and Ryland ( 1982 ) suggested that
gonochoristic zooids could have evolved as a result of
suppression or prolonged delay in the development of one
gonad in the course of the development of the other. If so, the
initial variant in colonial sexual structure would have been a
combination of sterile and hermaphrodite zooids, which is
the commonest mode of expression. This idea accords with
the hypotheses that hermaphroditism is the ancestral mode in
bilaterian animals (Balsamo 1992 ; Schmidt-Rhaesa 2007 )
and that the evolution of hermaphroditism is connected with
a sedentary way of life (Ghiselin 1969 , 1987 ), in which the
likelihood of gamete encounter is reduced in fi xed, spatially
separated colonies. In extreme cases, self-fertilization can be
resorted to (see below). On the other hand, Hughes et al.
( 2002a ) asked why hermaphroditism should be retained in
bryozoans if cross-fertilization is the rule. In further consideration of the potential challenge of achieving fertilization in
sedentary organisms, let me nevertheless note that, in a population of hermaphrodites, all individuals can reproduce
whereas only half can produce offspring in gonochoristic
populations. Moreover, hermaphroditism makes it possible
for a colony to manipulate resources, channelling them for
the production of either male or female gametes depending
on circumstances and thus increasing the probability of fertilization and the effi ciency of larval production (see also
Hughes et al. 2002a ).
1.2.1.1 Hermaphroditism and Cross-Fertilization
The co-occurrence of mature eggs and sperm in hermaphrodite zooids is common in gymnolaemates (Fig. 1. 34C ). It is
therefore not surprising that notions of intrazooidal selffertilization survived in the scientifi c literature until the
beginning of the twenty-fi rst century (Smith et al. 2003 ;
reviewed in Ostrovsky 2008b ; see also Sect. 1.3.6 and
Appendix I). Self-fertilization was assumed by Nordmann
( 1839 ), the fi rst to unambiguously describe sperm in
Bryozoa, and by van Beneden ( 1844a ) (see Sect. 1.1 ). The
former author, who studied Tendra zostericola , wrote that
spermatozoids entered the “female” zooids from “males” via
the opening in their base [supposedly, in the transverse wall],
thus implying the existence of intracolonial self-fertilization.
Van Beneden ( 1844a ) documented the co-occurrence of ripe
eggs and sperm in zooids of the ctenostome Farrella repens ,
and likewise assumed intrazooidal self-fertilization. Calvet
( 1900 ) even stated that he observed self-fertilization take
place in the zooid cavity in Bugula simplex .
As mentioned above, the fi rst researcher to dispute this
general opinion and to argue that cross-fertilization occurred
in some species, ctenostome as well as cheilostome, was
Joliet ( 1877 ). The existence of protandrous zooidal hermaphroditism and zooidal gonochorism, the massive production of spermatozoids, and their release and capability of
swimming actively in the surrounding water led him to
believe that cross-fertilization was the rule. This view was
strongly supported by the observations of Vigelius ( 1884b ),
who was one of the fi rst to describe the dynamics of sexual
changes in bryozoan colonies. Vigelius thought that sperm
release was possible through the zooidal aperture only after
polypide degeneration and destruction of the body wall.
Fertilization itself was supposed to occur externally,
inside the ovicell in brooding cheilostomes. However, the
co- occurrence of male and female gametes in the same
zooid forced him to admit the possibility of intrazooidal
self- fertilization in Bugula calathus (see Vigelius 1886 ).
Notwithstanding, neither Joliet nor Vigelius dwelt upon the
question of whether fertilization was intra- or intercolonial.
In this regard it should be noted that, since bryozoan populations consist of colonies of different age at different stages of
the sexual cycle, those that have only male or only female
gonads at the beginning of reproduction may participate only
in intercolonial cross-fertilization (see Ostrovsky 1998 ).
The discovery of precocious insemination (Marcus
1938a ) devalued the idea about the different timing of gonad
maturation in hermaphrodite zooids as an argument in favour
of cross-fertilization; i.e. if early oocytes can be fertilized in
the ovary, then the prior maturation of sperm in anticipation
of this event is clearly not an obstacle to intrazooidal selffertilization (see also Sect. 1.3.6 ).
The observations of Silén ( 1966 , 1972 ), Bullivant ( 1967 )
and Temkin ( 1994 ) on sperm release via the terminal pores
of the tentacles constituted direct evidence in favour of crossfertilization, as did data on the frequencies of allele distribution in natural populations (Schopf 1977 ; Thorpe et al.
1978a , b ; Thorpe and Beardmore 1981 ; see also Hoare et al.
1999 ). Cross-fertilization is also promoted by the relatively
long life of sperm (Manríquez et al. 2001 ), high effi ciency of
sperm capture by feeding lophophores (Temkin 1994 , 1996 ;
Pemberton et al. 2003 ), ability to store sperm by immature
colonies (Hughes et al. 2002a ) and the usually high population densities of the colonies (see also Hoare and Hughes
2001 ; Bishop and Pemberton 2006 and references therein).
Moreover, experiments with isolated colonies of Celleporella
hyalina showed that intracolonial self-fertilization in most
cases resulted in abortion of embryos, reduced larval fi tness
and low larval numbers (Cancino et al. 1991 ; Hunter and
Hughes 1993 , 1995 ; Hoare and Hughes 2001 ; Hughes et al.
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis