306
the lophophore. In his second paper on the “fertilization
problem”, Silén ( 1972 ) added eight cheilostome and two
cyclostome species to the list. It should be noted that only
malacostegan cheilostomes released their sperm via two
distomedial tentacles.
At approximately the same time, male heteromorphic
polypides were recorded in several Cheilostomata. The fi rst
observations on protruded male polypides were made by
Marcus ( 1938a ) in Celleporella sp., in which he counted six
tentacles (see above). Four tentacles were found in males of
Celleporella tongima (as Hippothoa ) (see Ryland and
Gordon 1977 ). In Odontoporella bishopi (as Hippopodinella
adpressa ), Gordon ( 1968 ) described male polypides with
four long and four short unciliated tentacles, with the characteristic “rocking” behaviour and not expanding in the usual
bell shape. Carter and Gordon ( 2007 ) also described the
male polypide as having a vestigial gut. Skeletally, these
zooids do not differ from others, possibly developing normal
feeding polypides after degeneration of the male ones.
Similarly, Cook ( 1968 ) recorded heteromorphic lophophores
in larger zooids, possessing three pairs of non-ciliated tentacles of different length, describing their behaviour in
Hippoporidra senegambiensis as rapid sweeps in one plane,
but in different directions, while protruded for 5–10 min.
Identical behaviour of four-tentacled male polypides was
recorded in H . littoralis (see Cook 1985 ). Groups of male
zooids with lophophores of two long non-ciliated tentacles
were also recorded in Hippoporidra sp.
Concerning sperm dispersal, Cook ( 1977 , 1979 ) suggested that the groups of male zooids may also act as passive
excurrent outlets. Chimonides and Cook ( 1981 ) observed
special behaviour of the elongated lophophores of paired,
unciliated tentacles in Selenaria maculata . These male
zooids develop on the periphery of the colony, and their
lophophores often protrude simultaneously in small groups.
Sections confi rmed the presence of sperm inside their zooid
cavity. Sperm were also found in several large ovarian
oocytes in the subperipheral female zooids. The zonal positioning of the differently sexed zooids corresponds with the
direction of the colonial water currents – sperm should be
removed from the colony without being captured by the
female zooids of the same colony. Detailed reviews on sexual zooidal polymorphism in Bryozoa have been published
by Silén ( 1977 ), who proposed a modifi ed terminology, and
by Cook ( 1979 ).
Franzén ( 1956 , 1970 , 1976 , 1977 , 1981 , 1983 , 1987a , b ,
1998 ) published a series of papers and reviews on bryozoan
sperm morphology and development and fertilization biology, analysing both his own results and those of others. In
passing, Franzén ( 1977 ) also briefl y described oocyte structure and oogenesis. Special attention was paid to comparing
sperm ultrastructure in the three main bryozoan groups,
Phylactolaemata, Stenolaemata and Gymnolaemata, the
results of which supported the hypothesis that latter two
classes are more closely related to each other than either is to
the Phylactolaemata. Franzén concluded that bryozoan
sperm is departs considerably from the morphology that he
considered representative of the primitive condition, which
is characteristic of external fertilization. According to his
hypothesis, bryozoan sperm morphology is indicative of
internal fertilization. Franzén ( 1956 , 1998 ) confi rmed
Bonnevie’s ( 1906 , 1907 ) fi ndings on the presence of spermatozeugmata in Membranipora membranacea and Electra
pilosa . Reger ( 1971 ) and Zimmer and Woollacott ( 1974 )
studied aspects of sperm ultrastructure in Bugula sp. and
Membranipora sp., respectively, and it was shown that spermatozeugmata consist of 32 or 64 spermatozoids in
Membranipora .
Woollacott and Zimmer ( 1972a ) redescribed the placental
analogue and confi rmed the data of previous authors on ooecial development from the distal zooid in Bugula neritina
(see discussion in Chap. 2 ). Woollacott and Zimmer ( 1972b ,
1975 ) also presented the results of a TEM investigation of
the placental system in this species. The embryophore was
reported to consist of two main elements – hypertrophied
epidermis of the ooecial vesicle and associated cells of the
funicular strands, presumably transporting nutrients for
embryo development. Сells of the embryo adjacent to the
embryophore are said to differentiate for nutrient uptake. At
the onset of brooding, the embryophore undergoes a dramatic transformation in size, cell structure and morphology,
and the funicular plexus enlarges to cover a large surface of
the basal ends of the hypertrophied cells, which show obvious signs of synthetic and transport activities. Apical parts of
the epidermal cells of both the ooecial vesicle and the embryo
are folded, developing microvilli (in the embryophore) and
infoldings (in the embryo) and performing exo- and pinocytosis, respectively. Woollacott and Zimmer suggested that
this transport might be bi-directional and that the embryophore could also accept waste from the embryo. It is particularly interesting that the transfer of matter occurs through the
cuticle of the ooecial vesicle, inferring diffusion or an
osmotic-gradient mechanism. The fertilization envelope surrounding the early embryo was not evident at an advanced
stage. The embryo increases ca. 500-fold in volume during
brooding. Woollacott and Zimmer ( 1975 , p. 363) also identifi ed three reproductive patterns “(planktonic, lecithotrophic
and placenta-like)” in Bryozoa.
In the 1960s and 1970s, research on bryozoan reproductive anatomy and behaviour was extended by the addition of
ecological studies (Kawahara 1960 ; Gautier 1962 ; Ryland
1963 ; Abbott 1973 , 1975 ; Hayward and Ryland 1975 –
reviewed in Ryland 1967 , 1970 , 1976 , and Soule and Soule
1977 )
. Among others are the papers of Gordon ( 1970 ) and
Eggleston ( 1963 , 1969 , 1972 ), who undertook investigations
on bryozoan reproductive ecology, studying their breeding
Appendices
the lophophore. In his second paper on the “fertilization
problem”, Silén ( 1972 ) added eight cheilostome and two
cyclostome species to the list. It should be noted that only
malacostegan cheilostomes released their sperm via two
distomedial tentacles.
At approximately the same time, male heteromorphic
polypides were recorded in several Cheilostomata. The fi rst
observations on protruded male polypides were made by
Marcus ( 1938a ) in Celleporella sp., in which he counted six
tentacles (see above). Four tentacles were found in males of
Celleporella tongima (as Hippothoa ) (see Ryland and
Gordon 1977 ). In Odontoporella bishopi (as Hippopodinella
adpressa ), Gordon ( 1968 ) described male polypides with
four long and four short unciliated tentacles, with the characteristic “rocking” behaviour and not expanding in the usual
bell shape. Carter and Gordon ( 2007 ) also described the
male polypide as having a vestigial gut. Skeletally, these
zooids do not differ from others, possibly developing normal
feeding polypides after degeneration of the male ones.
Similarly, Cook ( 1968 ) recorded heteromorphic lophophores
in larger zooids, possessing three pairs of non-ciliated tentacles of different length, describing their behaviour in
Hippoporidra senegambiensis as rapid sweeps in one plane,
but in different directions, while protruded for 5–10 min.
Identical behaviour of four-tentacled male polypides was
recorded in H . littoralis (see Cook 1985 ). Groups of male
zooids with lophophores of two long non-ciliated tentacles
were also recorded in Hippoporidra sp.
Concerning sperm dispersal, Cook ( 1977 , 1979 ) suggested that the groups of male zooids may also act as passive
excurrent outlets. Chimonides and Cook ( 1981 ) observed
special behaviour of the elongated lophophores of paired,
unciliated tentacles in Selenaria maculata . These male
zooids develop on the periphery of the colony, and their
lophophores often protrude simultaneously in small groups.
Sections confi rmed the presence of sperm inside their zooid
cavity. Sperm were also found in several large ovarian
oocytes in the subperipheral female zooids. The zonal positioning of the differently sexed zooids corresponds with the
direction of the colonial water currents – sperm should be
removed from the colony without being captured by the
female zooids of the same colony. Detailed reviews on sexual zooidal polymorphism in Bryozoa have been published
by Silén ( 1977 ), who proposed a modifi ed terminology, and
by Cook ( 1979 ).
Franzén ( 1956 , 1970 , 1976 , 1977 , 1981 , 1983 , 1987a , b ,
1998 ) published a series of papers and reviews on bryozoan
sperm morphology and development and fertilization biology, analysing both his own results and those of others. In
passing, Franzén ( 1977 ) also briefl y described oocyte structure and oogenesis. Special attention was paid to comparing
sperm ultrastructure in the three main bryozoan groups,
Phylactolaemata, Stenolaemata and Gymnolaemata, the
results of which supported the hypothesis that latter two
classes are more closely related to each other than either is to
the Phylactolaemata. Franzén concluded that bryozoan
sperm is departs considerably from the morphology that he
considered representative of the primitive condition, which
is characteristic of external fertilization. According to his
hypothesis, bryozoan sperm morphology is indicative of
internal fertilization. Franzén ( 1956 , 1998 ) confi rmed
Bonnevie’s ( 1906 , 1907 ) fi ndings on the presence of spermatozeugmata in Membranipora membranacea and Electra
pilosa . Reger ( 1971 ) and Zimmer and Woollacott ( 1974 )
studied aspects of sperm ultrastructure in Bugula sp. and
Membranipora sp., respectively, and it was shown that spermatozeugmata consist of 32 or 64 spermatozoids in
Membranipora .
Woollacott and Zimmer ( 1972a ) redescribed the placental
analogue and confi rmed the data of previous authors on ooecial development from the distal zooid in Bugula neritina
(see discussion in Chap. 2 ). Woollacott and Zimmer ( 1972b ,
1975 ) also presented the results of a TEM investigation of
the placental system in this species. The embryophore was
reported to consist of two main elements – hypertrophied
epidermis of the ooecial vesicle and associated cells of the
funicular strands, presumably transporting nutrients for
embryo development. Сells of the embryo adjacent to the
embryophore are said to differentiate for nutrient uptake. At
the onset of brooding, the embryophore undergoes a dramatic transformation in size, cell structure and morphology,
and the funicular plexus enlarges to cover a large surface of
the basal ends of the hypertrophied cells, which show obvious signs of synthetic and transport activities. Apical parts of
the epidermal cells of both the ooecial vesicle and the embryo
are folded, developing microvilli (in the embryophore) and
infoldings (in the embryo) and performing exo- and pinocytosis, respectively. Woollacott and Zimmer suggested that
this transport might be bi-directional and that the embryophore could also accept waste from the embryo. It is particularly interesting that the transfer of matter occurs through the
cuticle of the ooecial vesicle, inferring diffusion or an
osmotic-gradient mechanism. The fertilization envelope surrounding the early embryo was not evident at an advanced
stage. The embryo increases ca. 500-fold in volume during
brooding. Woollacott and Zimmer ( 1975 , p. 363) also identifi ed three reproductive patterns “(planktonic, lecithotrophic
and placenta-like)” in Bryozoa.
In the 1960s and 1970s, research on bryozoan reproductive anatomy and behaviour was extended by the addition of
ecological studies (Kawahara 1960 ; Gautier 1962 ; Ryland
1963 ; Abbott 1973 , 1975 ; Hayward and Ryland 1975 –
reviewed in Ryland 1967 , 1970 , 1976 , and Soule and Soule
1977 )
. Among others are the papers of Gordon ( 1970 ) and
Eggleston ( 1963 , 1969 , 1972 ), who undertook investigations
on bryozoan reproductive ecology, studying their breeding
Appendices