236
planktotrophic larva in the very earliest Ctenostomata
(before the origin of the Stenolaemata) was suggested by
Zimmer and Woollacott ( 1977b ) and Strathmann ( 1978a ).
Cyphonautes larvae are known in one of the least-derived
ctenostome superfamilies, the Alcyonidioidea (Todd 2000 ).
Moreover, the brood chambers of phylactolaemates are
formed on the oral side of the zooid, whereas in gymnolaemates they are formed on the anal side as noted by Silén
( 1944 ) (see also Jebram 1973 ). That is, these brood chambers are not homologous, which is another argument against
Silén’s hypothesis.
3.1.2 Other Consequences of Modifi cations
to Oogenesis
Other important consequences of the progressive accumulation of nutrients in oocytes could be: (1) a gradual decrease
in the number of eggs formed by a zooid; (2) a change in the
sequence of maturation of female gametes in the ovary (eggs
had to be formed one by one, not simultaneously in cohorts);
and (3) shortening of larval development. It also seems that
these processes were accompanied by changes in ovary
structure.
3.1.2.1 Decrease in the Number of Oocytes
As the amount of energy allocated for the production of a
single offspring increases, the total number of offspring necessarily decreases (Vance 1973 ; Smith and Fretwell 1974 ;
Strathmann 1985 ). In other words, the fewer oocytes that are
formed by the parent organism, the larger they are (Chia
1974 ; McEdward 1996 ; Marshall and Bolton 2007 ). Known
in many groups of marine invertebrates, this correlation is
also often connected with larval type and the presence or
absence of incubation of the progeny. For instance, phoronids with small oocytes (about 60 μm in diameter) are all
broadcasters, producing up to 500 eggs (1,000 and more in
Phoronopsis harmeri ) during the reproductive season. On
the other hand, phoronid species with large oocytes (100–
125 μm) are all brooders, producing 40–400 eggs, with the
size and the number being inversely correlated (Emig 1983 ;
Zimmer 1991 ). In both cases, feeding actinotroch larvae are
formed except in Phoronis ovalis , a brooder possessing the
largest oocytes and a non-feeding crawling larva. A similar
inverse correlation between egg size and egg number was
reported for brooding brittle stars (Byrne 1991a ) and opisthobranch molluscs of the genus Alderia that lay eggs in
clutches (Krug 1998 , 2007 ; Ellingson and Krug 2006 ; Krug
et al. 2007 ). In polychaetes of the genus Streblospio either
many (100–500 and more) small (70–90 μm) or a few (9–50)
large and “yolky” (100–200 μm) oocytes are produced
(Levin 1984 ). In both instances, embryos are brooded. Olive
( 1983 ) stated that, in polychaetes, an abundance of oocytes
means they are poor in yolk, whereas less numerous ones are
rich in nutrients.
The same trend is observed in bryozoans as well. All
species with non-feeding larvae are brooders generally
producing fewer larger eggs than broadcasters with their
planktotrophic larvae. Theoretically, if the amount of nutrients allocated for reproduction is stable, then the evolutionary increase of provisioning per one oocyte should lead,
taking into account the limited capacity of the gonad, to a
decrease in the number of oocytes. To provisionally assess
the productivity of fertile zooids in species with different
reproductive patterns, one may compare the number of
oocytes (ovarian, ovulated and brooded) per zooid at the time
of study, also considering the duration of the reproductive
season and, for brooding species, the duration of embryonic
incubation. For instance, larval development in the ovicell of
the calloporid cheilostome Callopora dumerilii takes about
two weeks (Silén 1945 ). In this way, 3–4 mature oocytes
may be successively formed in the ovary during the 1.5–2
months of the Swedish summer.
In most bryozoans the reproductive period lasts from one
to several months, with relatively few species reproducing
throughout the year (reviewed in Kuznetzov 1941 ; Borg
1947 ; Ryland 1963 , 1967 ; Gordon 1970 ; Eggleston 1963 ,
1972 ; Gautier 1962 ; Dyryndа and Ryland 1982 ; Seed and
Hughes 1992 ). The ovary is formed in the young zooid during the formation of the fi rst polypide and may function for a
long time, being “inherited” by several subsequent polypides
(Dyrynda and King 1983 ; Ostrovsky 1998c ; see also Sect.
1.2.1 ). In most species the ovary appears to be formed only
once in the zooid, whereas in some species it may be formed
at least twice, along with a regenerated polypide (Prouho
1892 ; Owrid and Ryland 1991 ). The life span of polypides in
different bryozoan species ranges from 6 to 72 days (Gordon
1977 ). Taking into account these features, we may try to
compare the productivity of broadcasting and brooding gymnolaemate Bryozoa. It should be kept in mind that the data
used are preliminary and very approximate. Oocyte size and
number were counted using either published illustrations
(often very schematic) made from living animals, or whole
preparations or anatomical sections. In the latter case, oocyte
numbers could be counted only in the plane of section so
their total number is clearly underestimated.
With the exception of Arbocuspis bellula , whose reproductive pattern is uncertain (see above), cheilostome broadcasters produce from 4–5 to 40–50 small oligolecithal
oocytes in a zooid at a given time (see Sect. 1.3.2 and
Table 3.1 ). In E . pilosa and M . membranacea fertile zooids
apparently produce oocytes over a long time period, at least
for several weeks and maybe for several months (Temkin,
M.H., 2002, personal communication; see also Eggleston
1963 ). This means that oogenesis continues after the ovulated
eggs have been spawned, and this is repeated several times.
3 Evolution of Reproductive Patterns in Cheilostomata
planktotrophic larva in the very earliest Ctenostomata
(before the origin of the Stenolaemata) was suggested by
Zimmer and Woollacott ( 1977b ) and Strathmann ( 1978a ).
Cyphonautes larvae are known in one of the least-derived
ctenostome superfamilies, the Alcyonidioidea (Todd 2000 ).
Moreover, the brood chambers of phylactolaemates are
formed on the oral side of the zooid, whereas in gymnolaemates they are formed on the anal side as noted by Silén
( 1944 ) (see also Jebram 1973 ). That is, these brood chambers are not homologous, which is another argument against
Silén’s hypothesis.
3.1.2 Other Consequences of Modifi cations
to Oogenesis
Other important consequences of the progressive accumulation of nutrients in oocytes could be: (1) a gradual decrease
in the number of eggs formed by a zooid; (2) a change in the
sequence of maturation of female gametes in the ovary (eggs
had to be formed one by one, not simultaneously in cohorts);
and (3) shortening of larval development. It also seems that
these processes were accompanied by changes in ovary
structure.
3.1.2.1 Decrease in the Number of Oocytes
As the amount of energy allocated for the production of a
single offspring increases, the total number of offspring necessarily decreases (Vance 1973 ; Smith and Fretwell 1974 ;
Strathmann 1985 ). In other words, the fewer oocytes that are
formed by the parent organism, the larger they are (Chia
1974 ; McEdward 1996 ; Marshall and Bolton 2007 ). Known
in many groups of marine invertebrates, this correlation is
also often connected with larval type and the presence or
absence of incubation of the progeny. For instance, phoronids with small oocytes (about 60 μm in diameter) are all
broadcasters, producing up to 500 eggs (1,000 and more in
Phoronopsis harmeri ) during the reproductive season. On
the other hand, phoronid species with large oocytes (100–
125 μm) are all brooders, producing 40–400 eggs, with the
size and the number being inversely correlated (Emig 1983 ;
Zimmer 1991 ). In both cases, feeding actinotroch larvae are
formed except in Phoronis ovalis , a brooder possessing the
largest oocytes and a non-feeding crawling larva. A similar
inverse correlation between egg size and egg number was
reported for brooding brittle stars (Byrne 1991a ) and opisthobranch molluscs of the genus Alderia that lay eggs in
clutches (Krug 1998 , 2007 ; Ellingson and Krug 2006 ; Krug
et al. 2007 ). In polychaetes of the genus Streblospio either
many (100–500 and more) small (70–90 μm) or a few (9–50)
large and “yolky” (100–200 μm) oocytes are produced
(Levin 1984 ). In both instances, embryos are brooded. Olive
( 1983 ) stated that, in polychaetes, an abundance of oocytes
means they are poor in yolk, whereas less numerous ones are
rich in nutrients.
The same trend is observed in bryozoans as well. All
species with non-feeding larvae are brooders generally
producing fewer larger eggs than broadcasters with their
planktotrophic larvae. Theoretically, if the amount of nutrients allocated for reproduction is stable, then the evolutionary increase of provisioning per one oocyte should lead,
taking into account the limited capacity of the gonad, to a
decrease in the number of oocytes. To provisionally assess
the productivity of fertile zooids in species with different
reproductive patterns, one may compare the number of
oocytes (ovarian, ovulated and brooded) per zooid at the time
of study, also considering the duration of the reproductive
season and, for brooding species, the duration of embryonic
incubation. For instance, larval development in the ovicell of
the calloporid cheilostome Callopora dumerilii takes about
two weeks (Silén 1945 ). In this way, 3–4 mature oocytes
may be successively formed in the ovary during the 1.5–2
months of the Swedish summer.
In most bryozoans the reproductive period lasts from one
to several months, with relatively few species reproducing
throughout the year (reviewed in Kuznetzov 1941 ; Borg
1947 ; Ryland 1963 , 1967 ; Gordon 1970 ; Eggleston 1963 ,
1972 ; Gautier 1962 ; Dyryndа and Ryland 1982 ; Seed and
Hughes 1992 ). The ovary is formed in the young zooid during the formation of the fi rst polypide and may function for a
long time, being “inherited” by several subsequent polypides
(Dyrynda and King 1983 ; Ostrovsky 1998c ; see also Sect.
1.2.1 ). In most species the ovary appears to be formed only
once in the zooid, whereas in some species it may be formed
at least twice, along with a regenerated polypide (Prouho
1892 ; Owrid and Ryland 1991 ). The life span of polypides in
different bryozoan species ranges from 6 to 72 days (Gordon
1977 ). Taking into account these features, we may try to
compare the productivity of broadcasting and brooding gymnolaemate Bryozoa. It should be kept in mind that the data
used are preliminary and very approximate. Oocyte size and
number were counted using either published illustrations
(often very schematic) made from living animals, or whole
preparations or anatomical sections. In the latter case, oocyte
numbers could be counted only in the plane of section so
their total number is clearly underestimated.
With the exception of Arbocuspis bellula , whose reproductive pattern is uncertain (see above), cheilostome broadcasters produce from 4–5 to 40–50 small oligolecithal
oocytes in a zooid at a given time (see Sect. 1.3.2 and
Table 3.1 ). In E . pilosa and M . membranacea fertile zooids
apparently produce oocytes over a long time period, at least
for several weeks and maybe for several months (Temkin,
M.H., 2002, personal communication; see also Eggleston
1963 ). This means that oogenesis continues after the ovulated
eggs have been spawned, and this is repeated several times.
3 Evolution of Reproductive Patterns in Cheilostomata