69
sexual products. In both ctenostomes and cheilostomes (see
above) it has the form of a ciliated funnel, lateral ridges and
ciliated gutter. A good argument for a former excretory function would be the occurrence of a SNP in sterile zooids also.
On the other hand, these internal ciliated structures might
have evolved de novo. Both scenarios suggest that the earliest Bryozoa could have inherited a pore leading from the
coelom to the exterior and used for evacuation of eggs (and
sperm?). As mentioned previously, a coelomopore is placed
near the tentacle base above the anus and leads to the
lophophoral coelom in Gymnolaemata, whereas it is at the
duplicature below the anus leading to the main coelom in
Phylactolaemata. It is, however, diffi cult to judge what this
difference might mean. Were they evolved independently in
these groups, and if not, which is the derived state?
The female gonopore later evolved into an ITO. The formation of this organ involved a contribution from the basal
parts of the two disto-medial tentacles that are closest to the
SNP. The process would involve the formation of two pairs
of lateral epithelial proliferations in the lower part of the tentacles; their fusion allowed for development of a new specialized tubular organ.
It should also be noted that, in contrast with the hypothesis of Silén ( 1945 ), this scenario requires fewer evolutionary
steps and corresponds to accepted ideas on the evolution of
bryozoan sexual reproduction (Boardman et al. 1983 ; Taylor
1988 ; Reed 1991 ; Ostrovsky and Taylor 2004 , 2005 ;
Ostrovsky 2009 , 2013 ; Ostrovsky et al. 2009a ).
1.3.9.3 Distribution of the ITO and SNP Among
Gymnolaemates
In the vast majority of cases, the ITO has been recorded in the
fertile (hermaphrodite and female) autozooids of broadcasting
(non-brooding) ctenostomes and cheilostomes (see Table 1.9 ).
In contrast, brooding species have no ITO, except for the
ctenostomes Alcyonidium duplex and Bulbella abscondita
(reduced ITO) and the cheilostomes Tendra zostericola and
Thalamoporella evelinae (Farre 1837 ; Prouho 1892 ; Braem
1951 ; Jebram and Everitt 1982 ; Paltschikowa- Ostroumowa
1926 ; Braiko 1967 ; Marcus 1941a ). Furthermore, two
ascophoran cheilostomes possess a special ovipositor reminiscent of the ITO. In Schizoretepora cf. pungens and
Schizoporella cf. errata “a movable fi nger-like tube” with a
tapered end is formed dorsally at the base of the lophophore
of the fertile zooid, originating from the extended introvert
just above the frontal surface of the colony (Maturo 1991b ,
pp. 572–573; Zimmer, personal communication, 2009). This
tube is described as being “very fl exible and contractile”, entering the brood chamber (ovicell) within which it would move
around fairly actively. The mature egg moves into the extended
tube, deforming like a “squirt of toothpaste” and is eventually
deposited into the ovicell. Apart from the six aforementioned
species, the remaining gymnolaemate brooders oviposit
through the supraneural coelomopore.
On the other hand, three broadcasting ctenostomes,
Farrella repens , Hypophorella expansa and Hislopia
malayensis release eggs via a coelomopore (Table 1.9 ).
Thus, most brooders possess a SNP and only a few species
have an ITO or its analogue. Vice versa, the majority of
broadcasters have an ITO and only three a SNP.
Bryozoans with an ITO tend to have multiserial colonies
that form large crusts, mats, anastomosing networks or
dense turfs of closely packed zooids, but the ctenostomes
Victorella pavida , Alcyonidium albidum and Arachnidium
fi brosum also have an ITO and can form not only dense
clumps (the fi rst species), sheets (the second species) and
dense patches of closely juxtaposed zooids (the third species), but also diffuse or uniserial chains (Prenant and Bobin
1956 ; Hayward 1985 ; De Blauwe 2009 ). Narrow encrusting
lobes are also formed in stellate colonies of electrid cheilostomes, which also have an ITO (Hincks 1880 , p. 137;
Prenant and Bobin 1956 , p. 201; Kluge 1975 ; Ryland and
Hayward 1977 ; Hayward and Ryland 1998 ). In contrast,
there are no known species with an ITO that have strictly
uniserial, runner-like colonial growth and diffuse chains of
zooids.
1.3.9.4 Evolution of the ITO in Relation
to Colonial Morphology
Reed ( 1991 ) suggested that the use of the terminal tentacle
pores for sperm release in Bryozoa provided a mechanism
by which the trapping of sperm by parent and adjacent
autozooids could be avoided. Could it be then that the tentacle pores acquired this function as a consequence of the
evolution of dense positioning of zooids in colonies? Could it
also follow that the ITO evolved in a similar way, elevating
the gonopore to a higher position in such a colony and
enhancing the chances of successful spawning of eggs
(as opposed to eggs being swallowed by the parent or neighbouring lophophore)?
In large, encrusting multiserial colonies, feeding polypides induce a broad column of descending water (Winston
1978 , 1979 ; Lidgard 1981 ; Dick 1987 ; Shunatova and
Ostrovsky 2002 ). In this situation, spawned oocytes in
broadcasting species are forced into the zone of high water
pressure that is created beneath the lophophores (Dick 1987 ;
Grünbaum 1995 ). This zone, especially in large colonies, is
characterized by a relatively low rate of water exchange.
Additionally, a proportion of the exhalant water is refi ltered
(Lidgard 1981 ; Grünbaum 1995 ; Shunatova and Ostrovsky
2001 , 2002 ; see also Ryland 2001 ). As a consequence of
these two processes, oocytes are at risk of being swallowed.
During observations of spawning in Electra pilosa , Borg
( 1926 ) recorded sequential transfer of released eggs from
lophophore to lophophore towards the colony periphery by
tentacle “claps” (see also Winston 1978 ; Shunatova and
Ostrovsky 2001 ). On the other hand, swallowing of oocytes
by maternal and neighbouring polypides has repeatedly
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
sexual products. In both ctenostomes and cheilostomes (see
above) it has the form of a ciliated funnel, lateral ridges and
ciliated gutter. A good argument for a former excretory function would be the occurrence of a SNP in sterile zooids also.
On the other hand, these internal ciliated structures might
have evolved de novo. Both scenarios suggest that the earliest Bryozoa could have inherited a pore leading from the
coelom to the exterior and used for evacuation of eggs (and
sperm?). As mentioned previously, a coelomopore is placed
near the tentacle base above the anus and leads to the
lophophoral coelom in Gymnolaemata, whereas it is at the
duplicature below the anus leading to the main coelom in
Phylactolaemata. It is, however, diffi cult to judge what this
difference might mean. Were they evolved independently in
these groups, and if not, which is the derived state?
The female gonopore later evolved into an ITO. The formation of this organ involved a contribution from the basal
parts of the two disto-medial tentacles that are closest to the
SNP. The process would involve the formation of two pairs
of lateral epithelial proliferations in the lower part of the tentacles; their fusion allowed for development of a new specialized tubular organ.
It should also be noted that, in contrast with the hypothesis of Silén ( 1945 ), this scenario requires fewer evolutionary
steps and corresponds to accepted ideas on the evolution of
bryozoan sexual reproduction (Boardman et al. 1983 ; Taylor
1988 ; Reed 1991 ; Ostrovsky and Taylor 2004 , 2005 ;
Ostrovsky 2009 , 2013 ; Ostrovsky et al. 2009a ).
1.3.9.3 Distribution of the ITO and SNP Among
Gymnolaemates
In the vast majority of cases, the ITO has been recorded in the
fertile (hermaphrodite and female) autozooids of broadcasting
(non-brooding) ctenostomes and cheilostomes (see Table 1.9 ).
In contrast, brooding species have no ITO, except for the
ctenostomes Alcyonidium duplex and Bulbella abscondita
(reduced ITO) and the cheilostomes Tendra zostericola and
Thalamoporella evelinae (Farre 1837 ; Prouho 1892 ; Braem
1951 ; Jebram and Everitt 1982 ; Paltschikowa- Ostroumowa
1926 ; Braiko 1967 ; Marcus 1941a ). Furthermore, two
ascophoran cheilostomes possess a special ovipositor reminiscent of the ITO. In Schizoretepora cf. pungens and
Schizoporella cf. errata “a movable fi nger-like tube” with a
tapered end is formed dorsally at the base of the lophophore
of the fertile zooid, originating from the extended introvert
just above the frontal surface of the colony (Maturo 1991b ,
pp. 572–573; Zimmer, personal communication, 2009). This
tube is described as being “very fl exible and contractile”, entering the brood chamber (ovicell) within which it would move
around fairly actively. The mature egg moves into the extended
tube, deforming like a “squirt of toothpaste” and is eventually
deposited into the ovicell. Apart from the six aforementioned
species, the remaining gymnolaemate brooders oviposit
through the supraneural coelomopore.
On the other hand, three broadcasting ctenostomes,
Farrella repens , Hypophorella expansa and Hislopia
malayensis release eggs via a coelomopore (Table 1.9 ).
Thus, most brooders possess a SNP and only a few species
have an ITO or its analogue. Vice versa, the majority of
broadcasters have an ITO and only three a SNP.
Bryozoans with an ITO tend to have multiserial colonies
that form large crusts, mats, anastomosing networks or
dense turfs of closely packed zooids, but the ctenostomes
Victorella pavida , Alcyonidium albidum and Arachnidium
fi brosum also have an ITO and can form not only dense
clumps (the fi rst species), sheets (the second species) and
dense patches of closely juxtaposed zooids (the third species), but also diffuse or uniserial chains (Prenant and Bobin
1956 ; Hayward 1985 ; De Blauwe 2009 ). Narrow encrusting
lobes are also formed in stellate colonies of electrid cheilostomes, which also have an ITO (Hincks 1880 , p. 137;
Prenant and Bobin 1956 , p. 201; Kluge 1975 ; Ryland and
Hayward 1977 ; Hayward and Ryland 1998 ). In contrast,
there are no known species with an ITO that have strictly
uniserial, runner-like colonial growth and diffuse chains of
zooids.
1.3.9.4 Evolution of the ITO in Relation
to Colonial Morphology
Reed ( 1991 ) suggested that the use of the terminal tentacle
pores for sperm release in Bryozoa provided a mechanism
by which the trapping of sperm by parent and adjacent
autozooids could be avoided. Could it be then that the tentacle pores acquired this function as a consequence of the
evolution of dense positioning of zooids in colonies? Could it
also follow that the ITO evolved in a similar way, elevating
the gonopore to a higher position in such a colony and
enhancing the chances of successful spawning of eggs
(as opposed to eggs being swallowed by the parent or neighbouring lophophore)?
In large, encrusting multiserial colonies, feeding polypides induce a broad column of descending water (Winston
1978 , 1979 ; Lidgard 1981 ; Dick 1987 ; Shunatova and
Ostrovsky 2002 ). In this situation, spawned oocytes in
broadcasting species are forced into the zone of high water
pressure that is created beneath the lophophores (Dick 1987 ;
Grünbaum 1995 ). This zone, especially in large colonies, is
characterized by a relatively low rate of water exchange.
Additionally, a proportion of the exhalant water is refi ltered
(Lidgard 1981 ; Grünbaum 1995 ; Shunatova and Ostrovsky
2001 , 2002 ; see also Ryland 2001 ). As a consequence of
these two processes, oocytes are at risk of being swallowed.
During observations of spawning in Electra pilosa , Borg
( 1926 ) recorded sequential transfer of released eggs from
lophophore to lophophore towards the colony periphery by
tentacle “claps” (see also Winston 1978 ; Shunatova and
Ostrovsky 2001 ). On the other hand, swallowing of oocytes
by maternal and neighbouring polypides has repeatedly
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata