256
period in cheilostome broadcasters (Dudley 1973 ). If so,
brood chambers must have evolved some time after the
beginning of accumulation of additional nutrients in oocytes.
In this regard, we may recall that some sea urchins and sea
stars have lecithotrophic larvae that are not brooded but
develop in the external environment (Pearse and Cameron
1991 ; Byrne 1991a , b , 1995 , Byrne and Cerra 1996 ; Jeffery
and Emlet 2003 ; see for review Levin and Bridges 1995 ).
Incipient parental care in some of the orders of these classes
is considered to be the next evolutionary step (Byrne and
Cerra 1996 ), although phylogenetic analysis shows that in
some cases Echinoidea evolved brooding while bypassing an
endotrophic free-swimming larval stage (Jeffery and Emlet
2003 ). All of these arguments taken together would seem to
lend support to the hypothesis that brooding evolved in bryozoans after the shift in oogenesis.
Whereas the vast majority of cheilostome brooders incubate just one embryo, in a few species brood chambers contain several embryos concurrently. Three to seven embryos
have been recorded in the ovicells of Scruparia chelata
(Hastings 1941 ; Mawatari 1973b ; Hayward and Ryland
1998 ), up to 10 in the acanthostegal brood chambers of
Tendra zostericola (see Braiko 1967 ), 2–3 in the ovicells of
Thalamoporella rozieri , four in T . californica and up to six at
various stages of development in T . evelinae (see Waters
1909 ; Hastings 1930 ; Marcus 1941a ; Chaney et al. 1989 ).
Three embryos of approximately the same size were seen in
the ovicells of Monoporella nodulifera ovicells (pers. obs).
Very large ovicells of Macropora levinseni (described by
Brown 1952 as M . grandis var. levinseni ) contain 2–4
embryos (Gordon 1970 ). I consider the presence of more
than one embryo in the brood chamber as a plesiomorphy,
characterizing early stages in the evolution of reproductive
pattern II, which originated on the basis of pattern I with
numerous oocytes. Notably, all of these bryozoans are representative of early anascan-cheilostome clades with primitive
brood chambers, which presumably evolved independently
( Macropora and Monoporella have true ovicells). Two
embryos have occasionally been reported in ovicells of
Schizoporella unicornis (of different age, judging by their
colour; see Ross and McCain 1976 ) and Bugula foliolata (as
B . fl abellata ) (Corrêa 1948 ), and from two to several embryos
were recorded in the internal brood sacs of Oshurkovia littoralis and Arctonula arctica (Eggleston 1972 ; pers. obs.). In
all of these cases, such multiple brooding may be considered
as an “atavism” from those times when the brood chamber
normally contained more than one embryo.
The above data are in accord with the suggestion that the
new (non-feeding) type of larva might have evolved rather
fast, while further increase in the size of oocytes was gradual. By way of illustration, the descriptions and drawings of
Repiahoff ( 1875 , 1878 ) show the oocytes of Tendra zostericola as having relatively little yolk (apparently mesolecithal)
and the endotrophic larva has a rudimentary non- functioning
gut (see also Ostroumov 1886b ). Compared to all other
endotrophic cheilostome larvae that have been studied, the
Tendra larva forms fastest. So, sexual reproduction in Tendra
zostericola appears to correspond to the early stages in the
evolution of the new reproductive pattern in Gymnolaemata.
As in malacostegans, (1) the zooid still forms numerous
oocytes in cohorts, (2) oocytes ovulate in a group and exit
the visceral coelom of the maternal zooid one by one with
the help of the intertentacular organ, and (3) oocytes are
small and contain few nutrients, so embryogenesis is rapid.
As in brooders, there is incubation in a brood chamber, but
(1) the brooding time is short, (2) incubation occurs in
groups, and (3) the larva has a non-functioning gut. As discussed above, with this set of both plesiomorphic and apomorphic characters brooding could have evolved before as
well as after the transition to lecithotrophy.
Gradual evolution towards large macrolecithal oocytes
with plentiful nutritive reserves could have had two consequences. Firstly, the duration of development up to the motile
larval stage was extended, as can be seen from a comparison
of the development time of T . zostericola larvae with the larvae of other brooders (see Sect. 3.1.2 ). The physiological
mechanisms of this phenomenon remain obscure, but a similar tendency (slower development rate with increasing oocyte
size) is observed in some other invertebrates, for instance,
decapods (Clarke 1982 ). However, for bryozoan embryos
developing in brood chambers, such prolongation of development was not risky.
Secondly, the number of simultaneously brooded embryos
gradually decreased to just one embryo. The antecedent multiple brooding mode was retained in only a few taxa. Some of
them, such as Thalamoporella , even have macrolecithal
oocytes (Marcus 1941a ). This combination of characters is
possible only if the brood cavity is very large, which is
indeed the case in Thalamoporella . The successively ripening macrolecithal oocytes appear to be transferred one by
one into the ovicell, which has room for several embryos.
Unfortunately, we have no information about oocyte type in
Scruparia , Macropora or Monoporella . Since Scruparia has
a lecithotrophic larva (and Macropora and Monoporella
almost certainly do as well), their oocytes should also have
an elevated nutrient content suffi cient for larval development
without feeding.
Three to seven oocytes are formed in the ovaries of the
malacostegan-like cheilostome “ Carbasea ” indivisa . After
ovulation they are transferred to the outside of the zooid and
brooded in clusters within external membranous sacs (Stach
1938 ), very similar to the situation in the ctenostome Triticella
fl ava (see above). In “ Carbasea ” indivisa and Tendra zostericola some of the embryos appear to develop faster than the
others (Paltschikowa-Ostroumowa 1926 ; Stach 1938 ), which
is probably due to a certain time gap in oviposition (the time
3 Evolution of Reproductive Patterns in Cheilostomata
period in cheilostome broadcasters (Dudley 1973 ). If so,
brood chambers must have evolved some time after the
beginning of accumulation of additional nutrients in oocytes.
In this regard, we may recall that some sea urchins and sea
stars have lecithotrophic larvae that are not brooded but
develop in the external environment (Pearse and Cameron
1991 ; Byrne 1991a , b , 1995 , Byrne and Cerra 1996 ; Jeffery
and Emlet 2003 ; see for review Levin and Bridges 1995 ).
Incipient parental care in some of the orders of these classes
is considered to be the next evolutionary step (Byrne and
Cerra 1996 ), although phylogenetic analysis shows that in
some cases Echinoidea evolved brooding while bypassing an
endotrophic free-swimming larval stage (Jeffery and Emlet
2003 ). All of these arguments taken together would seem to
lend support to the hypothesis that brooding evolved in bryozoans after the shift in oogenesis.
Whereas the vast majority of cheilostome brooders incubate just one embryo, in a few species brood chambers contain several embryos concurrently. Three to seven embryos
have been recorded in the ovicells of Scruparia chelata
(Hastings 1941 ; Mawatari 1973b ; Hayward and Ryland
1998 ), up to 10 in the acanthostegal brood chambers of
Tendra zostericola (see Braiko 1967 ), 2–3 in the ovicells of
Thalamoporella rozieri , four in T . californica and up to six at
various stages of development in T . evelinae (see Waters
1909 ; Hastings 1930 ; Marcus 1941a ; Chaney et al. 1989 ).
Three embryos of approximately the same size were seen in
the ovicells of Monoporella nodulifera ovicells (pers. obs).
Very large ovicells of Macropora levinseni (described by
Brown 1952 as M . grandis var. levinseni ) contain 2–4
embryos (Gordon 1970 ). I consider the presence of more
than one embryo in the brood chamber as a plesiomorphy,
characterizing early stages in the evolution of reproductive
pattern II, which originated on the basis of pattern I with
numerous oocytes. Notably, all of these bryozoans are representative of early anascan-cheilostome clades with primitive
brood chambers, which presumably evolved independently
( Macropora and Monoporella have true ovicells). Two
embryos have occasionally been reported in ovicells of
Schizoporella unicornis (of different age, judging by their
colour; see Ross and McCain 1976 ) and Bugula foliolata (as
B . fl abellata ) (Corrêa 1948 ), and from two to several embryos
were recorded in the internal brood sacs of Oshurkovia littoralis and Arctonula arctica (Eggleston 1972 ; pers. obs.). In
all of these cases, such multiple brooding may be considered
as an “atavism” from those times when the brood chamber
normally contained more than one embryo.
The above data are in accord with the suggestion that the
new (non-feeding) type of larva might have evolved rather
fast, while further increase in the size of oocytes was gradual. By way of illustration, the descriptions and drawings of
Repiahoff ( 1875 , 1878 ) show the oocytes of Tendra zostericola as having relatively little yolk (apparently mesolecithal)
and the endotrophic larva has a rudimentary non- functioning
gut (see also Ostroumov 1886b ). Compared to all other
endotrophic cheilostome larvae that have been studied, the
Tendra larva forms fastest. So, sexual reproduction in Tendra
zostericola appears to correspond to the early stages in the
evolution of the new reproductive pattern in Gymnolaemata.
As in malacostegans, (1) the zooid still forms numerous
oocytes in cohorts, (2) oocytes ovulate in a group and exit
the visceral coelom of the maternal zooid one by one with
the help of the intertentacular organ, and (3) oocytes are
small and contain few nutrients, so embryogenesis is rapid.
As in brooders, there is incubation in a brood chamber, but
(1) the brooding time is short, (2) incubation occurs in
groups, and (3) the larva has a non-functioning gut. As discussed above, with this set of both plesiomorphic and apomorphic characters brooding could have evolved before as
well as after the transition to lecithotrophy.
Gradual evolution towards large macrolecithal oocytes
with plentiful nutritive reserves could have had two consequences. Firstly, the duration of development up to the motile
larval stage was extended, as can be seen from a comparison
of the development time of T . zostericola larvae with the larvae of other brooders (see Sect. 3.1.2 ). The physiological
mechanisms of this phenomenon remain obscure, but a similar tendency (slower development rate with increasing oocyte
size) is observed in some other invertebrates, for instance,
decapods (Clarke 1982 ). However, for bryozoan embryos
developing in brood chambers, such prolongation of development was not risky.
Secondly, the number of simultaneously brooded embryos
gradually decreased to just one embryo. The antecedent multiple brooding mode was retained in only a few taxa. Some of
them, such as Thalamoporella , even have macrolecithal
oocytes (Marcus 1941a ). This combination of characters is
possible only if the brood cavity is very large, which is
indeed the case in Thalamoporella . The successively ripening macrolecithal oocytes appear to be transferred one by
one into the ovicell, which has room for several embryos.
Unfortunately, we have no information about oocyte type in
Scruparia , Macropora or Monoporella . Since Scruparia has
a lecithotrophic larva (and Macropora and Monoporella
almost certainly do as well), their oocytes should also have
an elevated nutrient content suffi cient for larval development
without feeding.
Three to seven oocytes are formed in the ovaries of the
malacostegan-like cheilostome “ Carbasea ” indivisa . After
ovulation they are transferred to the outside of the zooid and
brooded in clusters within external membranous sacs (Stach
1938 ), very similar to the situation in the ctenostome Triticella
fl ava (see above). In “ Carbasea ” indivisa and Tendra zostericola some of the embryos appear to develop faster than the
others (Paltschikowa-Ostroumowa 1926 ; Stach 1938 ), which
is probably due to a certain time gap in oviposition (the time
3 Evolution of Reproductive Patterns in Cheilostomata