5
Harmer’s generalizations, however, passed unnoticed,
and a long period elapsed before the three “modes of reproduction” in Bryozoa were rediscovered by Woollacott and
Zimmer ( 1975 , p. 363). Detailed defi nitions of these modes
were later given by Ryland ( 1982 ), Hageman ( 1983 ) and
Reed ( 1987 , 1991 ) (see also Ryland 1976 ; Dyrynda and
King 1982 , 1983 ; Woollacott 1999 ). Supplementing these
defi nitions with information on site and time of fertilization
(Temkin 1994 , 1996 ), as well as on oogenesis and brooding
(Ström 1977 ; Reed 1991 ), I propose to characterize the patterns of sexual reproduction in Bryozoa as follows.
Reproductive pattern I is found only in species belonging
to the most ancient cheilostome clade, Malacostegina, and in
several ctenostomes. It is characterized by simultaneous or
near-simultaneous maturation in the ovary of many/several
small oligolecithal oocytes that are fertilized in the cavity of
the maternal zooid directly during or shortly after ovulation,
ovulate in cohorts and are spawned into water. There is no
incubation, the embryo instead developing into a planktotrophic cyphonautes larva.
Reproductive pattern II is found in most Gymnolaemata.
It is characterized by near-simultaneous or successive
maturation in the ovary of many/several or few meso- or
macrolecithal oocytes of small, medium or large size, intraovarian fertilization and brooding of embryos (in groups or
sequentially one at a time) at the surface of the maternal zooid,
in the introvert of the polypide or in a specialized brood
chamber. The embryo develops into a lecithotrophic coronate
larva. In cheilostomes with this pattern the oocyte is paired
with its sibling, a nurse cell, and fertilization is precocious.
Reproductive pattern III is found in phylactolaemates and
by some representatives of both gymnolaemate orders. It is
characterized by near-simultaneous development of numerous small oligolecithal oocytes in phylactolaemates (but only
one is destined to be a larva) and by successive maturation in
the ovary of several oligo- or mesolecithal oocytes in gymnolaemates. Fertilization is intraovarian, embryos are brooded
(in groups or sequentially one at a time) in the introvert of the
polypide (in ctenostomes) or in brood chambers (in phylactolaemates, ctenostomes and cheilostomes). Brooding is
accompanied by extraembryonic nutrition. The embryo
develops into a non-feeding coronate larva. In cheilostomes
with this pattern the oocyte is paired with a nurse cell as it
develops in the ovary and fertilization is precocious.
The fusion of male and female pronuclei (karyogamy) is
always postponed until the oocyte has been removed from
the coelom of the maternal zooid (Temkin 1994 , 1996 ).
Thus, all three reproductive patterns are found in both
gymnolaemate orders. In general terms, the features of bryozoan reproductive pattern I are characteristic of an r-strategy
and those of patterns II and III, of a K-strategy. The main
difference between patterns II and III is in the way in which
nutrient reserves are transferred to the progeny – to the
oocyte in the ovary or to the embryo in the brood chamber
(lecithotrophic and placental strategies, see Kasyanov 1989 ).
It may be noted here that Dyrynda and Ryland ( 1982 , p. 241)
described the three aforementioned reproductive patterns of
bryozoans as “physiological reproductive categories”, but
this term has not been used since.
Thus, the characteristics important for descriptions of patterns of sexual reproduction are: (1) type, size and number of
oocytes and the sequence of their maturation; (2) site and
time of fertilization (syngamy); (3) presence or absence of
embryo incubation and, if present, its site; (4) presence or
absence of extraembryonic nutrition during incubation; and
(5) larval type.
Sexual reproduction of Bryozoa is not restricted to these
three patterns, however. A new pattern (pattern IV), recently
described in some cheilostomes, combines the features of
pattern II (macrolecithal oocytes) and of pattern III (extraembryonic nutrition) (Ostrovsky et al. 2009a ; Ostrovsky
2009 , 2013 ; Moosbrugger et al. 2012 ). Data in the literature
indicate that pattern IV may also be characteristic of some
ctenostomes (see Sect. 3.4.4 ).
Cheilostomes of the family Epistomiidae are viviparous,
and their embryonic development is accompanied by extraembryonic nutrition, with a single embryo developing from
the oligolecithal oocyte during reproduction in the coelomic
cavity of the fertile zooid (Dyrynda and King 1982 ).
Accordingly, this epistomiid variant merits the status of a
separate pattern, V. In cyclostome bryozoans, viviparity and
extraembryonic nutrition are accompanied by polyembryony
(summarized in Reed 1991 ). This variant can be considered
as reproductive pattern VI.
1.2.1 Sexual Structure of Colonies
Bryozoans are colonial hermaphrodites, with testes (spermatogenic tissue) and ovaries developing either within the
same zooid (zooidal hermaphroditism) or in different zooids
within the same colony (zooidal gonochorism). In some species there are gonochoristic and hermaphrodite zooids within
the same colony. In experiments conducted on the cyclostome Filicrisia geniculata in laboratory culture, colonies
behaved either as males or as females (Jenkins, personal
communication, 2012), but this seems to be an exception.
Thus, autozooids in a colony are sterile and sexual
(male, female and/or hermaphrodite). Sexual zooids can be
auto zooids or autozooidal polymorphs (Silén 1977 ). In gymnolaemates with zooidal hermaphroditism, autozooids may
be protandrous, protogynous or simultaneous hermaphrodites. In species with zooidal gonochorism, colonies may be
protandrous, protogynous or simultaneous hermaphrodites,
with male and female zooids sometimes exhibiting sexual
dimorphism. Morphological distinctions between male and
1.2 Reproductive Patterns of Bryozoa
Harmer’s generalizations, however, passed unnoticed,
and a long period elapsed before the three “modes of reproduction” in Bryozoa were rediscovered by Woollacott and
Zimmer ( 1975 , p. 363). Detailed defi nitions of these modes
were later given by Ryland ( 1982 ), Hageman ( 1983 ) and
Reed ( 1987 , 1991 ) (see also Ryland 1976 ; Dyrynda and
King 1982 , 1983 ; Woollacott 1999 ). Supplementing these
defi nitions with information on site and time of fertilization
(Temkin 1994 , 1996 ), as well as on oogenesis and brooding
(Ström 1977 ; Reed 1991 ), I propose to characterize the patterns of sexual reproduction in Bryozoa as follows.
Reproductive pattern I is found only in species belonging
to the most ancient cheilostome clade, Malacostegina, and in
several ctenostomes. It is characterized by simultaneous or
near-simultaneous maturation in the ovary of many/several
small oligolecithal oocytes that are fertilized in the cavity of
the maternal zooid directly during or shortly after ovulation,
ovulate in cohorts and are spawned into water. There is no
incubation, the embryo instead developing into a planktotrophic cyphonautes larva.
Reproductive pattern II is found in most Gymnolaemata.
It is characterized by near-simultaneous or successive
maturation in the ovary of many/several or few meso- or
macrolecithal oocytes of small, medium or large size, intraovarian fertilization and brooding of embryos (in groups or
sequentially one at a time) at the surface of the maternal zooid,
in the introvert of the polypide or in a specialized brood
chamber. The embryo develops into a lecithotrophic coronate
larva. In cheilostomes with this pattern the oocyte is paired
with its sibling, a nurse cell, and fertilization is precocious.
Reproductive pattern III is found in phylactolaemates and
by some representatives of both gymnolaemate orders. It is
characterized by near-simultaneous development of numerous small oligolecithal oocytes in phylactolaemates (but only
one is destined to be a larva) and by successive maturation in
the ovary of several oligo- or mesolecithal oocytes in gymnolaemates. Fertilization is intraovarian, embryos are brooded
(in groups or sequentially one at a time) in the introvert of the
polypide (in ctenostomes) or in brood chambers (in phylactolaemates, ctenostomes and cheilostomes). Brooding is
accompanied by extraembryonic nutrition. The embryo
develops into a non-feeding coronate larva. In cheilostomes
with this pattern the oocyte is paired with a nurse cell as it
develops in the ovary and fertilization is precocious.
The fusion of male and female pronuclei (karyogamy) is
always postponed until the oocyte has been removed from
the coelom of the maternal zooid (Temkin 1994 , 1996 ).
Thus, all three reproductive patterns are found in both
gymnolaemate orders. In general terms, the features of bryozoan reproductive pattern I are characteristic of an r-strategy
and those of patterns II and III, of a K-strategy. The main
difference between patterns II and III is in the way in which
nutrient reserves are transferred to the progeny – to the
oocyte in the ovary or to the embryo in the brood chamber
(lecithotrophic and placental strategies, see Kasyanov 1989 ).
It may be noted here that Dyrynda and Ryland ( 1982 , p. 241)
described the three aforementioned reproductive patterns of
bryozoans as “physiological reproductive categories”, but
this term has not been used since.
Thus, the characteristics important for descriptions of patterns of sexual reproduction are: (1) type, size and number of
oocytes and the sequence of their maturation; (2) site and
time of fertilization (syngamy); (3) presence or absence of
embryo incubation and, if present, its site; (4) presence or
absence of extraembryonic nutrition during incubation; and
(5) larval type.
Sexual reproduction of Bryozoa is not restricted to these
three patterns, however. A new pattern (pattern IV), recently
described in some cheilostomes, combines the features of
pattern II (macrolecithal oocytes) and of pattern III (extraembryonic nutrition) (Ostrovsky et al. 2009a ; Ostrovsky
2009 , 2013 ; Moosbrugger et al. 2012 ). Data in the literature
indicate that pattern IV may also be characteristic of some
ctenostomes (see Sect. 3.4.4 ).
Cheilostomes of the family Epistomiidae are viviparous,
and their embryonic development is accompanied by extraembryonic nutrition, with a single embryo developing from
the oligolecithal oocyte during reproduction in the coelomic
cavity of the fertile zooid (Dyrynda and King 1982 ).
Accordingly, this epistomiid variant merits the status of a
separate pattern, V. In cyclostome bryozoans, viviparity and
extraembryonic nutrition are accompanied by polyembryony
(summarized in Reed 1991 ). This variant can be considered
as reproductive pattern VI.
1.2.1 Sexual Structure of Colonies
Bryozoans are colonial hermaphrodites, with testes (spermatogenic tissue) and ovaries developing either within the
same zooid (zooidal hermaphroditism) or in different zooids
within the same colony (zooidal gonochorism). In some species there are gonochoristic and hermaphrodite zooids within
the same colony. In experiments conducted on the cyclostome Filicrisia geniculata in laboratory culture, colonies
behaved either as males or as females (Jenkins, personal
communication, 2012), but this seems to be an exception.
Thus, autozooids in a colony are sterile and sexual
(male, female and/or hermaphrodite). Sexual zooids can be
auto zooids or autozooidal polymorphs (Silén 1977 ). In gymnolaemates with zooidal hermaphroditism, autozooids may
be protandrous, protogynous or simultaneous hermaphrodites. In species with zooidal gonochorism, colonies may be
protandrous, protogynous or simultaneous hermaphrodites,
with male and female zooids sometimes exhibiting sexual
dimorphism. Morphological distinctions between male and
1.2 Reproductive Patterns of Bryozoa