65
ovicell. In contrast, in T . evelinae female polypides actively
feed as well as transfer eggs to the ovicell by a very large
intertentacular organ (Marcus 1941a ; see also below).
Gordon ( 1968a ) described dimorphic polypides in
Odontoporella bishopi (Hippoporidridae). In this species
there are four long and four short non-ciliated tentacles, held
erect instead of spread- apart, and rocking from side to side.
These polypides have a rudimentary gut (Carter and Gordon
2007 ). The cystids of these zooids, which contain spermatogenic tissue, are identical to those of adjacent autozooids and
it is possible that male polypides are substituted after degeneration by normal ones outside the reproductive period. In
Pacifi cincola insculpta (Pacifi cincolidae), a dwarf polypide
substitutes for a normal one in the female autozooid during
the formation of the fi rst oocyte (Nielsen 1981 ). The small
polypide is presumably used for obtaining sperm.
(4) In some species, sexual zooids differ in both polypide
and cystid morphology. Large cyclostome gonozooids
belong to this category, having a different shape, being typically much larger than autozooids and possessing a functional or rudimentary polypide in the early stage of the
development. Dwarf polypides were discovered by Levinsen
( 1902 ) in female polymorphs of cheilostome Didymozoum
simplex (Farciminariidae). They are presumably used for
obtaining sperm. In Celleporella hyalina (Hippothoidae),
sexual zooids are much smaller than sterile ones and the polypide is considerably reduced (Fig. 1.36A, B ); their cystids
are effectively gonad receptacles. On the other hand, the
diminution of female zooids is not refl ected in smaller ovicell or embryo size.
Actually, this species is one of the best exemplars of
sexual polymorphism. Its colonies consist of a basal layer
of sterile autozooids, with rare dwarf-male zooids between
them, as well as frontally budded sterile autozooids and
male and female polymorphs. Since the basal layer is the
fi rst to form, the colony is sterile in the beginning and then
becomes male. Then frontal budding results in the formation of a few sterile autozooids and male polymorphs.
Female polymorphs with ovicells appear later, developing
only by frontal budding. As soon as they appear, the colony
becomes hermaphrodite. Female zooids are mostly formed
centrifugally. Additionally, smaller sterile autozooids and
dwarf kenozooids (zooeciules) bud sporadically on the
frontal surface, so that the frontal layer may occupy the whole
surface of the colony except for two to three peripheral
rows of basal autozooids (Hughes 1987 ; Cancino and
Hughes 1988 ; Ostrovsky 1998 ).
Both male and female zooids of C . hyalina have dwarf
cystids and non-feeding rudimentary polypides without a gut
(Fig. 1.36A, B ). Female polypides have three non-ciliated
tentacles (two to three according to Marcus ( 1938a ), who
worked with two hippothoid species, however (see Ryland
( 1979 )). The fact that female zooids also have an ascus and
parietal musculature as well as an unpaired retractor muscle
indicates that the polypide may evert and retract, which
would be necessary to obtain sperm and, presumably, to perform oviposition (Ostrovsky 1998 ).
Marcus ( 1938a ) was the fi rst to observe live male zooids,
with expanded lophophores of six tentacles, in Celleporella
sp. (cf. Cancino and Hughes 1988 ). Four tentacles were
recorded in polypides of male zooids in Antarctothoa
tongima (Ryland and Gordon 1977 ). In C . hyalina , sperm are
released via the central (longest) tentacle of the male lophophore. If there are no external currents, sperm release is often
synchronized in a colony. Male tentacle crowns incline
towards ascending water movement, fi ltered and removed
from the colony by adjacent feeding lophophores (Hoare
et al. 1999 ; Manríquez et al. 2001 ).
In contrast, the so-called “cortical” zooids of Hippoporidra
senegambiensis (Hippoporidridae), with male heteromorphic
polypides, are larger than autozooids even though they possess very small orifi ces (Cook 1964b ). The male polypides
have six non-ciliated tentacles (three pairs of different length),
remain extended for 5–10 min, making quick strokes in the
same plane but in different directions (Cook 1968 , 1985 ). The
same behaviour was observed in the four- tentacled male polypides H . littoralis (Cook 1985 ), which have elongate polymorphic zooids with a very small orifi ce. Cook ( 1977 , 1985 )
suggested that groups of male zooids may be involved in passive removal of fi ltered water from the colony surface (socalled “passive chimneys”) [thus effectively removing sperm]
(see also Shunatova and Ostrovsky 2002 ; Ostrovsky and
Shunatova 2002 ). In Selenaria maculata (Selenariidae), the
male zooids that occur at the colony periphery, often in small
groups, each have a pair of long non-ciliated tentacles on a
long introvert. The tentacles expand for several seconds only
while making quick strokes (Chimonides and Cook 1981 ).
Female zooids, with a normal polypide, develop subperipherally, which prevents them from obtaining sperm formed in the
same colony, since fi ltered water is moved from the centre to
the periphery. Male, female and sterile zooids differ from
each other in the size and shape of the cystid.
Fertile zooids in Margaretta barbata (Margarettidae)
have a long, curved peristome, and their polypides with tentacles and a fully formed alimentary tract, are somewhat
smaller than those of other zooids.
Thus, the above-described morpho-functional specializations are expressed in the cystid, polypide or both. Cystids
may enlarge or diminish, sometimes also changing in shape.
In many cases, operculum size and shape change too. As for
polypides, their modifi cation may involve: (1) decrease in
overall size, (2) reduction in tentacle number, (3) loss of
cilia, (4) vestigialization of gut, and (5) acquisition of specialized behaviour. Judging from the distribution of sexual
polymorphs within the Cheilostomata, they evidently
evolved independently several times in different groups.
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
ovicell. In contrast, in T . evelinae female polypides actively
feed as well as transfer eggs to the ovicell by a very large
intertentacular organ (Marcus 1941a ; see also below).
Gordon ( 1968a ) described dimorphic polypides in
Odontoporella bishopi (Hippoporidridae). In this species
there are four long and four short non-ciliated tentacles, held
erect instead of spread- apart, and rocking from side to side.
These polypides have a rudimentary gut (Carter and Gordon
2007 ). The cystids of these zooids, which contain spermatogenic tissue, are identical to those of adjacent autozooids and
it is possible that male polypides are substituted after degeneration by normal ones outside the reproductive period. In
Pacifi cincola insculpta (Pacifi cincolidae), a dwarf polypide
substitutes for a normal one in the female autozooid during
the formation of the fi rst oocyte (Nielsen 1981 ). The small
polypide is presumably used for obtaining sperm.
(4) In some species, sexual zooids differ in both polypide
and cystid morphology. Large cyclostome gonozooids
belong to this category, having a different shape, being typically much larger than autozooids and possessing a functional or rudimentary polypide in the early stage of the
development. Dwarf polypides were discovered by Levinsen
( 1902 ) in female polymorphs of cheilostome Didymozoum
simplex (Farciminariidae). They are presumably used for
obtaining sperm. In Celleporella hyalina (Hippothoidae),
sexual zooids are much smaller than sterile ones and the polypide is considerably reduced (Fig. 1.36A, B ); their cystids
are effectively gonad receptacles. On the other hand, the
diminution of female zooids is not refl ected in smaller ovicell or embryo size.
Actually, this species is one of the best exemplars of
sexual polymorphism. Its colonies consist of a basal layer
of sterile autozooids, with rare dwarf-male zooids between
them, as well as frontally budded sterile autozooids and
male and female polymorphs. Since the basal layer is the
fi rst to form, the colony is sterile in the beginning and then
becomes male. Then frontal budding results in the formation of a few sterile autozooids and male polymorphs.
Female polymorphs with ovicells appear later, developing
only by frontal budding. As soon as they appear, the colony
becomes hermaphrodite. Female zooids are mostly formed
centrifugally. Additionally, smaller sterile autozooids and
dwarf kenozooids (zooeciules) bud sporadically on the
frontal surface, so that the frontal layer may occupy the whole
surface of the colony except for two to three peripheral
rows of basal autozooids (Hughes 1987 ; Cancino and
Hughes 1988 ; Ostrovsky 1998 ).
Both male and female zooids of C . hyalina have dwarf
cystids and non-feeding rudimentary polypides without a gut
(Fig. 1.36A, B ). Female polypides have three non-ciliated
tentacles (two to three according to Marcus ( 1938a ), who
worked with two hippothoid species, however (see Ryland
( 1979 )). The fact that female zooids also have an ascus and
parietal musculature as well as an unpaired retractor muscle
indicates that the polypide may evert and retract, which
would be necessary to obtain sperm and, presumably, to perform oviposition (Ostrovsky 1998 ).
Marcus ( 1938a ) was the fi rst to observe live male zooids,
with expanded lophophores of six tentacles, in Celleporella
sp. (cf. Cancino and Hughes 1988 ). Four tentacles were
recorded in polypides of male zooids in Antarctothoa
tongima (Ryland and Gordon 1977 ). In C . hyalina , sperm are
released via the central (longest) tentacle of the male lophophore. If there are no external currents, sperm release is often
synchronized in a colony. Male tentacle crowns incline
towards ascending water movement, fi ltered and removed
from the colony by adjacent feeding lophophores (Hoare
et al. 1999 ; Manríquez et al. 2001 ).
In contrast, the so-called “cortical” zooids of Hippoporidra
senegambiensis (Hippoporidridae), with male heteromorphic
polypides, are larger than autozooids even though they possess very small orifi ces (Cook 1964b ). The male polypides
have six non-ciliated tentacles (three pairs of different length),
remain extended for 5–10 min, making quick strokes in the
same plane but in different directions (Cook 1968 , 1985 ). The
same behaviour was observed in the four- tentacled male polypides H . littoralis (Cook 1985 ), which have elongate polymorphic zooids with a very small orifi ce. Cook ( 1977 , 1985 )
suggested that groups of male zooids may be involved in passive removal of fi ltered water from the colony surface (socalled “passive chimneys”) [thus effectively removing sperm]
(see also Shunatova and Ostrovsky 2002 ; Ostrovsky and
Shunatova 2002 ). In Selenaria maculata (Selenariidae), the
male zooids that occur at the colony periphery, often in small
groups, each have a pair of long non-ciliated tentacles on a
long introvert. The tentacles expand for several seconds only
while making quick strokes (Chimonides and Cook 1981 ).
Female zooids, with a normal polypide, develop subperipherally, which prevents them from obtaining sperm formed in the
same colony, since fi ltered water is moved from the centre to
the periphery. Male, female and sterile zooids differ from
each other in the size and shape of the cystid.
Fertile zooids in Margaretta barbata (Margarettidae)
have a long, curved peristome, and their polypides with tentacles and a fully formed alimentary tract, are somewhat
smaller than those of other zooids.
Thus, the above-described morpho-functional specializations are expressed in the cystid, polypide or both. Cystids
may enlarge or diminish, sometimes also changing in shape.
In many cases, operculum size and shape change too. As for
polypides, their modifi cation may involve: (1) decrease in
overall size, (2) reduction in tentacle number, (3) loss of
cilia, (4) vestigialization of gut, and (5) acquisition of specialized behaviour. Judging from the distribution of sexual
polymorphs within the Cheilostomata, they evidently
evolved independently several times in different groups.
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata