233
3.1.1.2 Examples Among Cheilostome Bryozoans
Data on female gametogenesis in cheilostome bryozoans
agree well with the above considerations. Differences in the
mode of oogenesis and oocyte size in species with different
reproductive patterns correlate with the presence of feeding
and non-feeding larval types in this group. Comparative data
on the size of oocytes in representatives of broadcasting
(with planktotrophic larva) and brooding (with lecithotrophic larvae) families of Cheilostomata are instructive. In
the majority of broadcasting cheilostomes (suborder
Malacostegina) the diameter of mature (ovulated) oocytes
is about 100 μm (measured in living specimens). In three
electrid species it is: from 80 to 105–178 μm in Electra
pilosa (see Marcus 1926a ; Temkin 1996 ), 100 × 70–80 μm in
Electra monostachys (Cook 1964 ; Hayward and Ryland
1998 ) and 110 μm in Einhornia crustulenta (see Cook 1962 ).
Species in two other malacostegine genera have similarsized oocytes: 85.8–101 μm in Membranipora serrilamella
(Hageman 1983 ; Mawatari 1975 ; Mawatari and Mawatari
1975 ), from 70 μm (Silén 1945 ) to 80–120 × 80 μm
(Eggleston 1963 ) and 100 μm (Temkin, personal communication, 2002) in M . membranacea , 100 μm in
M . isabelleana (Cancino et al. 1991 ), 85 μm in Conopeum
seurati (see Cook 1962 ) and 110 × 80 μm in C . reticulum
(see Cook 1964 ) (see also Sect. 1.3.2 and Table 3.1 ).
These data should be treated with caution, however.
Firstly, coelomic oocytes may increase in size, presumably,
because of water intake. If that is so, only late ovarian oocytes
can be compared. Secondly, different authors worked with
living or fi xed material, and fi xation can lead to change in
egg size. Thirdly, some of the measurements could have been
made without taking into account the shape of coelomic
oocytes, which are always fl attened in malacostegans. For
instance, in M . membranacea they measure 80–120 μm in
length, about 80 μm in width and 30 μm in depth (Eggleston
1963 ). Moreover, in Electra species ovulated eggs are
irregularly shaped (Prouho 1892 ; Calvet 1900 ; Marcus
1926a ; Mawatari 1975 ; Hageman 1983 ; Temkin, personal
communication, 2002).
The zygote of M . membranacea becomes rounded after
spawning, measuring about 60 μm in diameter (Temkin
1994 ). In M . serrilamella the diameter of the spherical
zygote after spawning does not exceed 50 μm (Mawatari
and Mawatari 1975 ). Approximately the same diameter,
65 × 45 μm, is characteristic of the expelled eggs of
Conopeum tenuissimum (Dudley 1973 ). Taking into account
that the size of coelomic oocytes in malacostegans is similar,
we may suppose that their size after spawning also does not
vary too much, falling within the range of 50–60 μm and
probably not exceeding 100 μm. For instance, average egg
length is 110 μm in Einchornia crustulenta , embryo size is
60 × 50 μm 12 h after release (Cook 1962 ).
Most species in the family Calloporidae, the most ancient
family of brooding cheilostomes, which probably evolved
from a malacostegine ancestor, have larger oocytes than
species of electrids and membraniporids (see Table 1.6 ).
Among the calloporids studied, oocytes are relatively small
(75 × 45 µm in diameter) only in Crassimarginatella sp.
In most calloporids, however, their diameter is more than
100 μm, attaining 195 × 128 μm in Tegella armifera .
Importantly, calloporid oocytes are among the smallest in
cheilostomes with lecithotrophic larvae. In the overwhelming
majority of such cheilostomes (with reproductive patterns II
and IV), oocyte diameter is greater than in malacostegans,
ranging from 100 to 400 μm (see Sect. 1.2.4 and Table 1.6 ),
and only a few of them produce oocytes smaller than 100 μm
diameter. Thus, this situation parallels the above-mentioned
correlation between oocyte size and larval type recorded in
polychaetes and echinoids, pointing to a common theme in
the evolution of these invertebrate groups.
Considering together the features of oogenesis and ovarian
structure in living species as well as the time of origination of
taxa with different reproductive patterns in the geochronological record, we may be fairly sure that the fi rst cheilostomes (Malacostegina), which evolved in the Jurassic, had
pattern I of sexual reproduction with numerous small oocytes
developing into exotrophic cyphonautes larvae. The evolution
of brooding cheilostomes in the Cretaceous was based on the
transition to reproductive pattern II in which there are fewer
oocytes having greater size and nutrient reserves and endotrophic larvae developing in brood chambers.
In species with planktotrophic larvae, the oocyte in the
ovary receives a reserve of nutrients that are mostly spent
on the development of the egg itself and on embryogenesis,
including the formation of ciliary locomotion, the foodcapturing apparatus and the larval gut. As the malacostegan
embryo is capable of movement before it starts feeding
(Cook 1962 ; Mawatari 1975 ), some of the energy obtained
from the parent organism is also spent on this early movement. After the formation of the gut, the early larva “fends
for itself”. So, it may develop further, swim, settle and
metamorphose only if it obtains nutrients and energy by
actively feeding.
Accumulation of additional nutrient reserves, accompanied by egg enlargement, should result in a decrease of the
larval swimming (and feeding) period. For instance, feeding
larvae with a short development phase were described in
some echinoderms (Hoegh-Guldberg and Pearse 1995 ), and
it can be suggested that they illustrate the early stage of transition to endotrophy. A further step might be facultative
planktotrophy.
In Bryozoa, in accordance with the general trend, as soon
as the amount of nutrients and energy supplied by the parent
organism was completely suffi cient for larval development
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
3.1.1.2 Examples Among Cheilostome Bryozoans
Data on female gametogenesis in cheilostome bryozoans
agree well with the above considerations. Differences in the
mode of oogenesis and oocyte size in species with different
reproductive patterns correlate with the presence of feeding
and non-feeding larval types in this group. Comparative data
on the size of oocytes in representatives of broadcasting
(with planktotrophic larva) and brooding (with lecithotrophic larvae) families of Cheilostomata are instructive. In
the majority of broadcasting cheilostomes (suborder
Malacostegina) the diameter of mature (ovulated) oocytes
is about 100 μm (measured in living specimens). In three
electrid species it is: from 80 to 105–178 μm in Electra
pilosa (see Marcus 1926a ; Temkin 1996 ), 100 × 70–80 μm in
Electra monostachys (Cook 1964 ; Hayward and Ryland
1998 ) and 110 μm in Einhornia crustulenta (see Cook 1962 ).
Species in two other malacostegine genera have similarsized oocytes: 85.8–101 μm in Membranipora serrilamella
(Hageman 1983 ; Mawatari 1975 ; Mawatari and Mawatari
1975 ), from 70 μm (Silén 1945 ) to 80–120 × 80 μm
(Eggleston 1963 ) and 100 μm (Temkin, personal communication, 2002) in M . membranacea , 100 μm in
M . isabelleana (Cancino et al. 1991 ), 85 μm in Conopeum
seurati (see Cook 1962 ) and 110 × 80 μm in C . reticulum
(see Cook 1964 ) (see also Sect. 1.3.2 and Table 3.1 ).
These data should be treated with caution, however.
Firstly, coelomic oocytes may increase in size, presumably,
because of water intake. If that is so, only late ovarian oocytes
can be compared. Secondly, different authors worked with
living or fi xed material, and fi xation can lead to change in
egg size. Thirdly, some of the measurements could have been
made without taking into account the shape of coelomic
oocytes, which are always fl attened in malacostegans. For
instance, in M . membranacea they measure 80–120 μm in
length, about 80 μm in width and 30 μm in depth (Eggleston
1963 ). Moreover, in Electra species ovulated eggs are
irregularly shaped (Prouho 1892 ; Calvet 1900 ; Marcus
1926a ; Mawatari 1975 ; Hageman 1983 ; Temkin, personal
communication, 2002).
The zygote of M . membranacea becomes rounded after
spawning, measuring about 60 μm in diameter (Temkin
1994 ). In M . serrilamella the diameter of the spherical
zygote after spawning does not exceed 50 μm (Mawatari
and Mawatari 1975 ). Approximately the same diameter,
65 × 45 μm, is characteristic of the expelled eggs of
Conopeum tenuissimum (Dudley 1973 ). Taking into account
that the size of coelomic oocytes in malacostegans is similar,
we may suppose that their size after spawning also does not
vary too much, falling within the range of 50–60 μm and
probably not exceeding 100 μm. For instance, average egg
length is 110 μm in Einchornia crustulenta , embryo size is
60 × 50 μm 12 h after release (Cook 1962 ).
Most species in the family Calloporidae, the most ancient
family of brooding cheilostomes, which probably evolved
from a malacostegine ancestor, have larger oocytes than
species of electrids and membraniporids (see Table 1.6 ).
Among the calloporids studied, oocytes are relatively small
(75 × 45 µm in diameter) only in Crassimarginatella sp.
In most calloporids, however, their diameter is more than
100 μm, attaining 195 × 128 μm in Tegella armifera .
Importantly, calloporid oocytes are among the smallest in
cheilostomes with lecithotrophic larvae. In the overwhelming
majority of such cheilostomes (with reproductive patterns II
and IV), oocyte diameter is greater than in malacostegans,
ranging from 100 to 400 μm (see Sect. 1.2.4 and Table 1.6 ),
and only a few of them produce oocytes smaller than 100 μm
diameter. Thus, this situation parallels the above-mentioned
correlation between oocyte size and larval type recorded in
polychaetes and echinoids, pointing to a common theme in
the evolution of these invertebrate groups.
Considering together the features of oogenesis and ovarian
structure in living species as well as the time of origination of
taxa with different reproductive patterns in the geochronological record, we may be fairly sure that the fi rst cheilostomes (Malacostegina), which evolved in the Jurassic, had
pattern I of sexual reproduction with numerous small oocytes
developing into exotrophic cyphonautes larvae. The evolution
of brooding cheilostomes in the Cretaceous was based on the
transition to reproductive pattern II in which there are fewer
oocytes having greater size and nutrient reserves and endotrophic larvae developing in brood chambers.
In species with planktotrophic larvae, the oocyte in the
ovary receives a reserve of nutrients that are mostly spent
on the development of the egg itself and on embryogenesis,
including the formation of ciliary locomotion, the foodcapturing apparatus and the larval gut. As the malacostegan
embryo is capable of movement before it starts feeding
(Cook 1962 ; Mawatari 1975 ), some of the energy obtained
from the parent organism is also spent on this early movement. After the formation of the gut, the early larva “fends
for itself”. So, it may develop further, swim, settle and
metamorphose only if it obtains nutrients and energy by
actively feeding.
Accumulation of additional nutrient reserves, accompanied by egg enlargement, should result in a decrease of the
larval swimming (and feeding) period. For instance, feeding
larvae with a short development phase were described in
some echinoderms (Hoegh-Guldberg and Pearse 1995 ), and
it can be suggested that they illustrate the early stage of transition to endotrophy. A further step might be facultative
planktotrophy.
In Bryozoa, in accordance with the general trend, as soon
as the amount of nutrients and energy supplied by the parent
organism was completely suffi cient for larval development
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences