260
development of a non-feeding larva. Fertile zooids of
Triticella fl ava were observed to contain up to 60 mature
ovulated oocytes, some or many of which are brooded while
attached to the maternal zooid (Ström 1969 ). Apart from
possessing numerous small eggs and the simplest brooding
type, the primitive nature of this reproductive variant is indicated by the fact that the larva has a non-functioning gut.
The evolution of pattern II was apparently linked with the
reduction in the number of oocytes reaching maturation (and,
subsequently, brooded embryos), even while eggs were still
forming in the ovary in relatively large numbers (see
Table 3.2 ). Species illustrating this trend also show a tendency towards successive release of gametes and brooding of
embryos. For instance, one (rarely two) embryos are brooded
on the thread attached to the base of the introvert of the
maternal zooid in Pottsiella erecta (Smith et al. 2003 ), while
ovarian oocytes in this species number over 20, including
four mature ones 160 μm diameter (Smith et al. 2003 ).
External brooding has also been described in Paludicella
articulata (see Braem 1896 ), however the data on reproduction in this species are inadequate for comparison.
External brooding of embryos attached to the maternal
zooid is also known in Bulbella abscondita , Panolicella
nutans and Alcyonidium duplex (Prouho 1892 ; Braem 1951 ;
Jebram 1985 ). These species seem to exhibit the trend
towards a decrease in the number of female gametes in the
ovary. Whereas B . abscondita and A . duplex form about 10
oocytes and simultaneously brood 3–7 embryos, P . nutans
forms 5–6 oocytes and broods 2–5 embryos. Mature oocytes
are small (70–100 μm diameter). In addition, in these three
species the developing embryos are withdrawn into the vestibulum together with the polypide during its retraction
(hence representing a “mixed” type of brooding; see
Ostrovsky and Porter 2011 ). Interestingly, in P . nutans not
all the embryos are drawn into the introvert; this depends on
their position of attachment. In B . abscondita and A . duplex
the polypide attaches the eggs to the vestibulum wall by the
intertentacular organ. The combination of brooding and the
intertentacular organ is evidence that brooding species
evolved from non-brooding ones.
Tanganella appendiculata and T . muelleri have up to 13
(the former) or 19 (the latter) small ovarian oocytes 80–95 μm
diameter, which mature, are released and are brooded in
small groups (from 1–3 to 6), being immersed into the vestibular wall of the maternal zooid (Braem 1951 ; Jebram and
Everitt 1982 ). In this case, the still relatively large number of
oocytes is combined with a more advanced (as compared to
the previously considered) type of brooding in the invagination of the body wall (discussed by Braem 1951 ). Notably,
all but one ( Pottsiella erecta ) of the above-mentioned species
has small eggs ≤ 100 μm diameter.
(2) Brooding in invaginations of the cystid wall was a prerequisite of the origin of placental analogues and extraembryonic nutrition in ctenostomes. The result was a
considerable enlargement of the embryos. Prouho ( 1892 ),
for instance, recorded a difference in size among three
brooded embryos in Nolella dilatata . Despite their small
number (1–3), this species produces about 90 small eggs in
the ovary. Similarly, Labiostomella gisleni broods just one
embryo while producing over a 100 oocytes in the ovary.
Only a maximum of 10 ovulate after reaching 70 μm diameter, being further accumulated in the coelom (Silén 1944 ).
A single embryo is also brooded in Sundanella sibogae
(Braem 1940 ). In the two latter species the structure of the
brood sac wall points to it being a placental analogue. This
fact plus embryonic enlargement and the small oocytes indicate that these species have reproductive pattern III. Thus, it
may be conjectured that, in ctenostomes, pattern III is derived
from pattern II and not from pattern IV, as presumably happened in Cheilostomata. Although incubating only one to a
few embryos, these species still produce numerous, relatively small (oligo- or mesolecithal) oocytes. Interestingly,
this reproductive variant appears to be also characteristic of
all freshwater bryozoans. The fact that Labiostomella and
Sundanella (together with Nolella ) belong to different ctenostome superfamilies means that matrotrophic incubation
evolved in them independently.
(3) An additional variant in the evolution of brooding in
ctenostomes was the transition to embryonic incubation in
the introvert. The initial step for this mode may have been
external brooding. In Alcyonidium duplex (superfamily
Alcyonidioidea), several embryos develop simultaneously
while attached to the base of the introvert, being retracted
into it and protracted with it concurrent with the feeding
activities of the polypide. A similar mode is known in B .
abscondita . The next stage is the obligatory degeneration of
the polypide during the female phase of the zooidal cycle, so
that embryos are brooded in the introvert, which is sometimes modifi ed: 4–11 embryos are brooded simultaneously
in Alcyonidium hirsutum ; 6–12 in A . eightsi ; 4–6 in A . polyoum ; 4–5 in Pherusella tubulosa ; 4–5 in A . diaphanum ; and
3–4 in A . gelatinosum (Owrid and Ryland 1991 ; Seed and
Hughes 1992 ; Porter and Hayward 2004 ; Porter et al. 2001 ;
Porter 2004 ; Ryland and Porter 2006 ; Prouho 1892 ). A single embryo forming from very large oocyte (330–370 μm
diameter) develops in A . disciforme (Kuklinski and Porter
2004 ). It seems that there is no correlation between a
decrease in the number of brooded embryos and an increase
in size of the oocytes; for instance, in A . eightsi (6–12
embryos) large oocytes can exceed 300 μm diameter (see
also Table 3.2 ).
In all of these species with reproductive pattern II, mature
oocytes are transferred into the cavity of the introvert, modifi ed to become a brood chamber, without any assistance from
the polypide. In A . polyoum a special incubation pouch
develops instead of the degenerated tentacle sheath (Matricon
3 Evolution of Reproductive Patterns in Cheilostomata
development of a non-feeding larva. Fertile zooids of
Triticella fl ava were observed to contain up to 60 mature
ovulated oocytes, some or many of which are brooded while
attached to the maternal zooid (Ström 1969 ). Apart from
possessing numerous small eggs and the simplest brooding
type, the primitive nature of this reproductive variant is indicated by the fact that the larva has a non-functioning gut.
The evolution of pattern II was apparently linked with the
reduction in the number of oocytes reaching maturation (and,
subsequently, brooded embryos), even while eggs were still
forming in the ovary in relatively large numbers (see
Table 3.2 ). Species illustrating this trend also show a tendency towards successive release of gametes and brooding of
embryos. For instance, one (rarely two) embryos are brooded
on the thread attached to the base of the introvert of the
maternal zooid in Pottsiella erecta (Smith et al. 2003 ), while
ovarian oocytes in this species number over 20, including
four mature ones 160 μm diameter (Smith et al. 2003 ).
External brooding has also been described in Paludicella
articulata (see Braem 1896 ), however the data on reproduction in this species are inadequate for comparison.
External brooding of embryos attached to the maternal
zooid is also known in Bulbella abscondita , Panolicella
nutans and Alcyonidium duplex (Prouho 1892 ; Braem 1951 ;
Jebram 1985 ). These species seem to exhibit the trend
towards a decrease in the number of female gametes in the
ovary. Whereas B . abscondita and A . duplex form about 10
oocytes and simultaneously brood 3–7 embryos, P . nutans
forms 5–6 oocytes and broods 2–5 embryos. Mature oocytes
are small (70–100 μm diameter). In addition, in these three
species the developing embryos are withdrawn into the vestibulum together with the polypide during its retraction
(hence representing a “mixed” type of brooding; see
Ostrovsky and Porter 2011 ). Interestingly, in P . nutans not
all the embryos are drawn into the introvert; this depends on
their position of attachment. In B . abscondita and A . duplex
the polypide attaches the eggs to the vestibulum wall by the
intertentacular organ. The combination of brooding and the
intertentacular organ is evidence that brooding species
evolved from non-brooding ones.
Tanganella appendiculata and T . muelleri have up to 13
(the former) or 19 (the latter) small ovarian oocytes 80–95 μm
diameter, which mature, are released and are brooded in
small groups (from 1–3 to 6), being immersed into the vestibular wall of the maternal zooid (Braem 1951 ; Jebram and
Everitt 1982 ). In this case, the still relatively large number of
oocytes is combined with a more advanced (as compared to
the previously considered) type of brooding in the invagination of the body wall (discussed by Braem 1951 ). Notably,
all but one ( Pottsiella erecta ) of the above-mentioned species
has small eggs ≤ 100 μm diameter.
(2) Brooding in invaginations of the cystid wall was a prerequisite of the origin of placental analogues and extraembryonic nutrition in ctenostomes. The result was a
considerable enlargement of the embryos. Prouho ( 1892 ),
for instance, recorded a difference in size among three
brooded embryos in Nolella dilatata . Despite their small
number (1–3), this species produces about 90 small eggs in
the ovary. Similarly, Labiostomella gisleni broods just one
embryo while producing over a 100 oocytes in the ovary.
Only a maximum of 10 ovulate after reaching 70 μm diameter, being further accumulated in the coelom (Silén 1944 ).
A single embryo is also brooded in Sundanella sibogae
(Braem 1940 ). In the two latter species the structure of the
brood sac wall points to it being a placental analogue. This
fact plus embryonic enlargement and the small oocytes indicate that these species have reproductive pattern III. Thus, it
may be conjectured that, in ctenostomes, pattern III is derived
from pattern II and not from pattern IV, as presumably happened in Cheilostomata. Although incubating only one to a
few embryos, these species still produce numerous, relatively small (oligo- or mesolecithal) oocytes. Interestingly,
this reproductive variant appears to be also characteristic of
all freshwater bryozoans. The fact that Labiostomella and
Sundanella (together with Nolella ) belong to different ctenostome superfamilies means that matrotrophic incubation
evolved in them independently.
(3) An additional variant in the evolution of brooding in
ctenostomes was the transition to embryonic incubation in
the introvert. The initial step for this mode may have been
external brooding. In Alcyonidium duplex (superfamily
Alcyonidioidea), several embryos develop simultaneously
while attached to the base of the introvert, being retracted
into it and protracted with it concurrent with the feeding
activities of the polypide. A similar mode is known in B .
abscondita . The next stage is the obligatory degeneration of
the polypide during the female phase of the zooidal cycle, so
that embryos are brooded in the introvert, which is sometimes modifi ed: 4–11 embryos are brooded simultaneously
in Alcyonidium hirsutum ; 6–12 in A . eightsi ; 4–6 in A . polyoum ; 4–5 in Pherusella tubulosa ; 4–5 in A . diaphanum ; and
3–4 in A . gelatinosum (Owrid and Ryland 1991 ; Seed and
Hughes 1992 ; Porter and Hayward 2004 ; Porter et al. 2001 ;
Porter 2004 ; Ryland and Porter 2006 ; Prouho 1892 ). A single embryo forming from very large oocyte (330–370 μm
diameter) develops in A . disciforme (Kuklinski and Porter
2004 ). It seems that there is no correlation between a
decrease in the number of brooded embryos and an increase
in size of the oocytes; for instance, in A . eightsi (6–12
embryos) large oocytes can exceed 300 μm diameter (see
also Table 3.2 ).
In all of these species with reproductive pattern II, mature
oocytes are transferred into the cavity of the introvert, modifi ed to become a brood chamber, without any assistance from
the polypide. In A . polyoum a special incubation pouch
develops instead of the degenerated tentacle sheath (Matricon
3 Evolution of Reproductive Patterns in Cheilostomata