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229
A. Ostrovsky, Evolution of Sexual Reproduction in Marine Invertebrates: Example of gymnolaemate bryozoans,
DOI 10.1007/978-94-007-7146-8_3, © Springer Science+Business Media Dordrecht 2013
Abstract
This chapter contains an analysis of the main directions in the evolution of sexual reproduction
in bryozoans – changes in modes of oogenesis and fertilization, the transition from plank-
totrophy to a non-feeding larva and its consequences, the origin of embryo incubation, and
the repeated evolution of matrotrophy and placental analogues. The trends that emerge from
this analysis are compared with reproductive analogues in the evolution of the bryozoan
order Ctenostomata as well as other marine invertebrate groups (predominantly echino-
derms, molluscs and polychaetes). The conditions under which the cheilostomes radiated in
the Late Cretaceous are considered in detail, and the consequences of the transitions to new
reproductive patterns are analyzed. It is suggested that a shift in oogenesis (reduction in egg
number and increase in their size) and parental care can apparently evolve in Cheilostomata
sequentially, with a short time lag: oogenesis becomes modifi ed fi rst, with the decrease in
the number of offspring compensated soon after by the origin of brooding. Finally, the
stages in the evolution of sexual reproduction in other bryozoan groups (classes
Phylactolaemata and Stenolaemata) are reconstructed.
Keywords
Brooding • Evolution • Fertilization • Lecithotrophy • Oogenesis • Placentotrophy
• Planktotrophy
Evolution of Reproductive Patterns
in Cheilostomata 3
The evolution of skeletal brood chambers (ovicells) in
cheilostome bryozoans coincided with the onset of their
radiation in the Late Cretaceous, which has been attributed to
the origin of the new larval type (Taylor 1988a ). The transi-
tion from a planktotrophic to a lecithotrophic larva was
apparently due to a shift in oogenesis. In extant species of the
most ancient cheilostome families (suborder Malacostegina)
there is no brooding and numerous small oligolecithal eggs
after internal fertilization are spawned to the water column
where they develop into feeding cyphonautes larvae (sexual
reproduction pattern I). In contrast, living cheilostome
brooders produce relatively few macrolecithal oocytes that
are generally larger than the oocytes of broadcasting cheilo-
stomes and accumulate a suffi cient amount of nutrient
reserves to complete larval development without feeding
(pattern II). Thus, a shift from oligo- to macrolecithal
oogenesis should be a necessary precondition for the evolu-
tion of a non-feeding larva. Further changes led to the origin
of extraembryonic nutrition and placental analogues in some
cheilostome lineages. Finally, most resources were allocated
to the larva at the stage of embryogenesis, and oogenesis
changed back again from macro- to oligolecithal (as demon-
strated in species with patterns IV and III).
The discussion that follows deals with the evolution
of advanced patterns of sexual reproduction, accompa-
nied by shifts in oogenesis, multiple origins of embry-
onic incubation and the evolution of the endotrophic
larva in cheilostome bryozoans. Questions of particular
interest in this respect are the prerequisites and the early
stages of the transition to endotrophy, a connection, if
any, between the change in oogenesis mode and the origin of
brooding, and the role of fertilization and extraembry-
onic nutrition in further transformations of the reproduc-
tive patterns.
230
3.1 Modifi cation of Oogenesis and
Its Evolutionary Consequences
3.1.1 Changes in Oogenesis and Evolution
of the Lecithotrophic Larva
3.1.1.1 General Remarks
Planktotrophy is considered as the primitive state of the
larval phase in the life cycle of marine invertebrates
(Jägersten 1972 ; Strathmann 1978a , b ; Nielsen 1998 , 2013 ;
Levin and Bridges 1995 ; Wray 1995a ), though there are
strong arguments supporting the opinion that the fi rst larval
forms of early metazoans were non-feeding (von Salvini-
Plawen 1982 ; Haszprunar et al. 1995 ; Peterson 2005 ; Nützel
et al. 2006 ; see also Strathmann 1993 ). Still, planktotrophic
larvae are very ancient, and it is generally accepted that the
transition to endotrophy occurred repeatedly in many marine
phyla (Jägersten 1972 ; Strathmann 1975 , 1978a , 1985 , 1986 ,
1993 ; Wray 1995a ; McEdward and Janies 1997 ; Nielsen
1998 , 2013 ; Peterson 2005 and references therein). For
instance, in the phylum Echinodermata this transition
occurred at least 35 times (Emlet et al. 1987 ; Wray 1995a )
and within the sea star family Asterinidae lecithotrophy
originated independently six times (Byrne 2006 ).
Hypothetical consequences of the evolution of non-
feeding larva are discussed in numerous publications (see
Chia 1974 ; Strathmann 1978a , 1980 , 1985 ; Jablonski and
Lutz 1983 ; Jablonski 1986 ; Emlet et al. 1987 ; Poulin and
Féral 1996 and references therein). On the whole, such larvae,
with their lesser dependence on external conditions and
lesser risk of mortality because of a generally shorter swim-
ming period, are considered as an alternative to wider-
dispersing larvae with a prolonged feeding in the plankton.
The necessity of dispersal vs the “expediency” of progeny
settling in the biotopes where the parents live has also been
broadly discussed (for reviews see Strathmann 1985 ;
Kasyanov
1989 ; Reed 1991 ; Knowlton and Jackson 1993 ;
Havenhand
1995 ).
There are a number of hypotheses discussing ecological
factors that might trigger the transition from exotrophy to
endotrophy (reviewed in Strathmann 1985 , 1986 ; Havenhand
1995 ; Levin and Bridges 1995 ). For instance, fl uctuations in
phytoplankton abundance owing to climatic seasonality are
often considered. When the amount of food accessible to
planktotrophic larvae fl uctuates abruptly, a transition to
lecithotrophy does seem benefi cial (McNamara 1994 ; Poulin
and Féral 1996 ; Jeffery 1997 ; McEdward and Miner 2003 ;
see also Valentine 1986 ). This hypothesis is rooted in
Thorson’s rule (so-called), suggesting that planktotrophic
development is rare in cold (i.e. polar and deep) waters.
(Thorson 1950 ; Mileikovsky 1971 ; Clarke 1992 ; Jablonski
and Lutz
1983 ; Kasyanov 1989 ). Although Thorson’s rule
itself was strongly criticized (Chia 1974 ; Clark and Goetzfried
1978 ; Pearse 1994 ; Pearse and Bosch 1994 ; see also Levin and
Bridges 1995 and Marshall et al. 2012 ), a correlation between
trophic limitations and the shift to a non-feeding larva still
seems theoretically reasonable (Clarke 1992 ; Jeffery 1997 ).
Other hypotheses explain a loss of planktotrophy by
seasonal freshening of surface waters after ice melting, low
temperatures (in high latitudes) and dispersal features, etc.
(discussed in Poulin and Féral 1996 ). According to Chia
( 1974 ), transition to lecithotrophy can be a forced response
to having to survive conditions of acute resource shortage for
adults. In this case a decrease in the number of offspring is
effi cacious, being offset by larger offspring size and thus
lesser vulnerability to predation. Nielsen ( 1995 , 1998 )
argued that non-feeding larvae could have evolved as a result
of competition and/or predation in the plankton. Todd and
Doyle (
1981 ) suggested that the evolution of new larval
types could be associated with the timing of reproduction
and settlement periods in relation to seasons having an
increased amount of food available to parents and juveniles,
the type of larva and the duration of its development
depending on the availability of food for the juvenile (see
also Havenhand
1993 ).
The above hypotheses suggest that ecology drives the shift
in larval type. But what are the intrinsic mechanisms behind
this shift? It has been accepted relatively recently that “it is
during oogenesis that the developmental program is altered
and saved both in terms of nuclear genetic information and in
the cytoplasmic organization of the egg” (Raff and Kaufman
1983 ; Wourms 1987 , p. 52; Wray and Raff 1991 ; Raff 1996 ;
see also Prowse and Byrne 2012 ) and that the transition from
one larval type to another involves correlated changes in
oogenesis, embryogenesis and larval development (Wray and
Raff 1990 , 1991 ; Wray 1992 ; Eckelbarger 1994 ).
Whatever the ecological factors and selective regimes in
the evolution of a non-feeding mode of development, the
necessary step in this direction was modifi cation of oogene-
sis via an increase in the maternal provisioning that resulted
in a larger, nutrient-rich oocyte (Wray and Raff 1991 ; Jaeckle
1995 ; Byrne et al. 2003 ). Chia ( 1974 ) and Strathmann and
co-authors ( 1992 ) noted that the evolution of lecithotrophy
might be explained by an increase in the energy input of
the parent organism into oocyte development. In this way,
the offspring would have been provisioned with suffi cient
reserves to complete development without feeding
(Mortensen 1921 ; Havenhand 1995 ; Wray 1995a ). As a
result, the larvae formed from large oocytes no longer
needed structures for capture and digestion of food particles
(Strathmann 1978a , 1993 ). As Strathmann ( 1975 , p. 727)
wrote: “if an egg is supplied with suffi cient reserves so that
feeding is no longer required for completion of larval
development, then selection will no longer eliminate many
mutations affecting the development of the larval body.”
3 Evolution of Reproductive Patterns in Cheilostomata
231
The transition from a planktotrophic to a lecithotrophic
larva and direct development in sea urchins, brittle stars and
sea stars, along with associated changes in embryogenesis,
larval morphology and ecology, were analyzed in detail in the
works of Byrne (
1991a , b ), Wray ( 1996 ), Hart ( 1996 ) and
McEdward and Janies (
1993 , 1997 ) (see also McEdward
2000 ; McEdward and Miner 2001 ; Byrne 2006 ). An interme-
diate stage between feeding and non-feeding modes might be
a form of facultative planktotrophy, known in a number of
invertebrates (discussed in Havenhand 1995 ; Hart 1996 ).
Vance’s ( 1973 ) mathematical model predicts that such a stage
would be of short duration at the geological scale because it is
evolutionarily less successful, as indicated by the fact that
such examples are rare (see also Emlet et al. 1987 ; Wray and
Raff 1991 ; Wray 1995a , 1996 ). It is also possible that their
apparent rarity (as the consequence of a relatively short
evolutionary existence) is because such species either give
rise to species with non-feeding larvae or become extinct
(Wray and Raff 1991 ). Conversely, Emlet ( 1986 ) thought that
facultative planktotrophy may be stable from an evolutionary
viewpoint, as such larvae may profi t from the positive attri-
butes of both developmental variants (Emlet et al. 1987 ;
Havenhand 1995 ; McEdward 1997 ; Allen and Pernet 2007 ;
for a detailed discussion see Hart 1996 ). Wray ( 1996 )
remarked that such larvae are effi cacious only under quite
specifi c conditions. Whatever the case, it is facultative plank-
totrophy (which according to some researchers is more com-
mon than generally thought) that illustrates the transition
from one state to the other (Kempf and Hadfi eld 1985 ; Emlet
1986 ; McEdward 1996 , 1997 ; Allen and Pernet 2007 ).
Among invertebrates, facultative planktotrophy is known
in two sea urchins, four gastropods, a bivalve and a poly-
chaete (Perron 1981 ; Alatalo et al. 1984 ; Kempf and Hadfi eld
1985 ; Emlet 1986 ; Kempf and Todd 1989 ; Miller 1993 ; Hart
1996 ; Pernet and McArthur 2006 ; reviewed in Wray and
Raff 1991 ; Havenhand 1995 ; Wray 1995a ; Raff 1996 ;
Hadfi eld and Strathmann 1996 ). For instance, females of the
polychaete Streblospio benedicti (Atlantic population) form
two types of eggs (small and large), from which, correspond-
ingly, planktotrophic and facultatively planktotrophic larvae
develop. An individual female produces only one type of
oocytes, yet females of different “types” coexist side by side
in the same sites throughout the year. Females from the
Pacifi c population of the same species form only facultative
planktotrophic larvae (Pernet and McArthur 2006 ).
In general, accumulation of additional resources infl u-
ences oocyte size. Havenhand ( 1995 ) and Wray ( 1996 )
considered increase in egg size to be a factor determining the
transition to facultative larval feeding. As egg reserves reach
the threshold required for completion of metamorphosis, this
increase should result in obligate lecithotrophy; many
authors have pointed to the correlation between larval
type and the size of the oocytes from which they develop.
Although this correlation is not strict, an increase in egg size
generally “seems to be both necessary and suffi cient for
completion of metamorphosis without feeding” (reviewed in
Strathmann
1978a , 1993 ; Todd and Doyle 1981 ; Emlet et al.
1987 ; Wray and Raff 1991 ; Wray 1995a , p. 428; Raff 1996 ;
Moran and McAlister
2009 ; see also below).
Thorson ( 1950 ) was one of the fi rst to note the connection
between oocyte size and larval-development type: within a
phylum, small eggs usually develop into planktotrophic
larvae, while large eggs develop into endotrophic larvae or
undergo direct development. Indeed, oocyte size often reli-
ably predicts larval type (Strathmann 1985 ; Jaeckle 1995 ;
Wray 1995a ). In polychaetes of the genus Streblospio , for
instance, oocytes less than 70 μm diameter develop into
planktotrophic larvae and oocytes more than 120 μm into
lecithotrophic larvae. Eggs 200 μm diameter transform
directly into juveniles (reviewed in Levin and Bridges
1995 ).
A similar tendency has been noted within Echinodermata in
general and Echinoidea in particular. In sea urchins, plankto-
trophic plutei larvae develop from oocytes 65–320 μm diam-
eter, lecithotrophic larvae similar to plutei from oocytes
300–500 μm diameter, strongly modifi ed lecithotrophic lar-
vae from oocytes 400–1,200 μm diameter, and if oocytes
reach 1–2 cm in diameter development is direct (Wray and
Raff
1991 ; Wray 1995a ; Raff 1996 ; Kasyanov 1989 ; Emlet
1990 ; reviewed in Emlet et al. 1987 ). Similar correlations
were recorded in asterinid sea stars in which planktotrophic
larvae develop from 150 to 170 μm eggs and lecithotrophic
ones from 320 to 1,000 μm eggs (reviewed in Emlet et al.
1987 ; Byrne 2006 ; see also Levin and Bridges 1995 ; Jaeckle
1995 ). The larger the oocyte, the fewer traces of planktotro-
phy are exhibited in echinoderm lecithotrophic larvae (Pearse
and Cameron 1991 ). The same correlation has been ascer-
tained in nudibranch and bivalve molluscs (discussed in
Todd and Doyle 1981 ; Kasyanov 1989 ; Kasyanov et al.
1998 ), and phoronids (Emig 1983 ; Zimmer 1991 ). A similar
correlation was recently shown for Annelida, Echinodermata
and Mollusca by Marshall et al. (
2012 ).
In this connection, the experiments of Sinervo and
McEdward (
1988 ) on blastomeres of sea urchins with
planktotrophic development should also be mentioned.
Development of embryos from isolated blastomeres taken
after the fi rst and second divisions (correspondingly ½ and ¼
of zygote volume) of the larger of two congeneric species,
Strongylocentrotus droebachiensis , was slower than the
development of the embryo from the zygote and resulted in a
smaller, simpler larva, comparable with that of the smaller
species S . purpuratus . This means that the size of the initial
cell directly infl uenced the rate and outcome of development.
These authors concluded that the very fact of evolutionary
changes in egg size could be a factor determining the shape
and functions of the larva. According with this conclusion are
the data of Hart (
1996 ), supporting the hypothesis that, in the
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
232
transition from feeding to non-feeding mode, evolution of
large eggs precedes any modifi cations in larval development.
However, this rule does not appear to be very strict. There
are cases among sea urchins in which non-feeding larvae
develop from smaller oocytes, whereas echinoplutei develop
from larger ones (Emlet et al. 1987 ; Bosch 1989 ; Wray and
Raff
1991 ; Hoegh-Guldberg and Pearse 1995 ). To sum up,
there is a general correlation between larger eggs and leci-
thotrophy but there are exceptions. This conclusion is sup-
ported by experimental embryological data: in the sea urchin
Peronella japonica a lecithotrophic larva develops from each
of the two blastomeres separated after the fi rst division (as it
does from the normal embryo), though these blastomeres are
much smaller than the oocytes of planktotrophic species
(Okazaki and Dan 1954 ; Wray and Raff 1991 ; summarized
in Jaeckle 1995 ). A similar situation obtains for half-embryos
resulting from bisection along the second cleavage plane of
Heliocidaris erythrogramma (Henry and Raff 1990 ; Wray
and Raff 1991 ). The developmental programme appears to
be genetically determined in these species.
Oocytes of invertebrates differ not only in size but also in
the content of a particular nutrient per unit volume, with
small oocytes being characterized by higher concentrations
than large ones in echinoderms with feeding larvae
(Strathmann and Vedder 1977 ). Thus, differences between
two contrasting developmental modes cannot be simply
explained by the absolute size of the egg. What is very
important is the amount of organic content (McEdward and
Carson 1987 ) and biochemical composition (Jaeckle 1995 ),
hence egg volume is not simply proportional to its energy
content (Emlet et al. 1987 ; Eckelbarger 1994 ). It has been
shown in echinoderms that planktotrophic larvae develop
from the oocytes that mostly accumulate proteins, while leci-
thotrophic ones develop from those that accumulate lipids.
The evolution of large eggs, in concert with transition to the
preferred and progressive accumulation of lipids in oocytes,
is considered to be an important aspect of the transformation
of oogenesis during evolution of lecithotrophic larvae (Wray
and Raff 1991 ; Byrne et al. 1999 , 2003 ; Byrne and Cerra
2000 ; Villinski et al. 2002 ; Wray 2002 ; Falkner et al. 2006 ;
Prowse et al. 2008 , 2009 ).
According to Christiansen and Fenchel ( 1979 ), the transi-
tion from one developmental type to the other may be rather
fast by geological standards, as little as several million years
(see also Wray and Raff 1991 ; Wray 1995a , b ). This transi-
tion was accomplished in four to seven million years in two
clades of sea urchins living on different sides of the Isthmus
of Panama (Zigler et al. 2003 ; Jeffery et al. 2003 , discussed in
Raff and Byrne 2006 ). Moreover, Hart et al. ( 1997 ) presented
molecular data showing that it might take less than two
million years in sea stars. Strathmann and Eernisse ( 1994 )
agreed that an increase in nutritional reserves in the ovum
would permit rapid evolutionary changes in larval form.
Instances of congeneric species having exo- and endotrophic
larvae are well-known in sea urchins, sea stars, polychaetes,
ctenostome bryozoans and some other invertebrates;
moreover, in some opisthobranch gastropods and poly-
chaetes these two types of larvae may be found within the
same species (poecilogony) (Zimmer and Woollacott
1977a ; Clark et al. 1979 ; Hoagland and Robertson 1988 ;
Pearse and Cameron 1991 ; Wray and Raff 1991 ; Byrne
1991b , 2006 ; Byrne and Barker 1991 ; Levin and Bridges
1995 ; Havenhand 1995 ; Raff 1996 ; Hart 1996 ; Byrne et al.
1999 ; Gibson and Gibson 2004 ; Krug 2007 ). These
instances indicate that the switch from one oogenesis
type to the other, which occurred repeatedly in the history
of different groups and hence from one larval type to the
other, is not a very diffi cult evolutionary step. A striking
example is provided by the snail Alderia willowi , which
shifts oogenesis (and hence larval type) depending on the
season: numerous small eggs from which long-living
planktotrophic larvae develop are produced in winter and
spring, whereas a few large eggs from which lecithotrophic
larvae develop are laid in summer. Moreover, some non-
feeding larvae undergo metamorphosis immediately after
hatching and some settle only 2–4 days later. In addition,
the same snails may switch from one type of oogenesis
(and larva) to the other (Ellingson and Krug 2006 ; Krug 2007 ;
Krug et al. 2007 ).
In discussing genetic changes behind the loss of larval
characters, Nielsen ( 1998 , p. 144) wrote that there might be
only a single mutation in larval development “which turns
off the regulatory gene”. In contrast, Strathmann with co-
authors ( 1992 ) inferred that the main reason is a genetic
change in the programming of oogenesis. It was shown in
experiments using sea urchin planktotrophic larvae that
abundance of food results in both shortening of development
time and changes in the structure and development of the
plutei. Moreover, such plutei structurally and developmen-
tally resembled sea urchin endotrophic larvae. This pheno-
typic plasticity was considered as a preadaptation in the
transition to a non-feeding larva. Based on this, Strathmann
and coauthors ( 1992 ) suggested that regardless of whether
nutrient resources are exo- or endogenous an increase in
their amount would result in structural changes in the larvae
enabling the fastest possible competence. In their opinion,
since the plentiful food available for planktotrophic larvae
results in changes characteristic of lecithotrophic ones, the
transition to non-feeding larvae does not require genetic
changes relating to embryogenesis and larval development.
Changes in the genetic programme of oogenesis that result
in an increase in the amount of nutrients in the oocytes is
suffi cient. According to Wray and Raff (
1991 ), the necessary
prerequisite for a transition to a new larval type is the “weak-
ening” of the pressure of stabilizing selection and the accu-
mulation of mutations.
3 Evolution of Reproductive Patterns in Cheilostomata
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 lecithotro-
phic 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 similar-
sized 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 com-
munication, 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 geochrono-
logical record, we may be fairly sure that the fi rst cheilo-
stomes (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 endotro-
phic 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 food-
capturing 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 move-
ment. 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, accompa-
nied 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 tran-
sition 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
234
Table 3.1 Number and size of ovarian and ovulated coelomic oocytes and expelled eggs, size of cyphonautes larvae and ancestrulae in species of
Malacostegina (based on literature data)
Species
Oocyte number
(ovarian/
ovulated)
Ovulated oocytes
or expelled eggs
(diameter, μm)
Mature
cyphonautes
(μm) Ancestrula (μm) References
Conopeum tenuissimum −/5–6 65.0 × 45.0 (expelled
egg)
200.0 × 140.0 Dudley ( 1973 )
Conopeum seurati 85.0 Cook ( 1962 )
180.0 × 160.0 200.0–220.0 × 140.0–150.0 Cook and
Hayward (
1966 )
Conopeum reticulum −/5–9 110.0 × 80.0 290.0 × 200.0 220.0 × 130.0 Cook ( 1964 )
Einhornia crustulenta −/6 Silén ( 1966 )
−/16 Borg ( 1947 )
160.0–200.0
× 150.0
250.0 × 130.0 Cook ( 1960 )
110.0 Cook ( 1962 )
160.0–240.0
× 120.0–170.0
Ryland ( 1965 )
Electra monostachys −/5–9 100.0 × 70.0 250.0 × 150.0 180.0–240.0 × 100.0–200.0 Cook ( 1964 )
260.0 × 165.0 Ryland ( 1965 )
100.0 × 80.0 Hayward and
Ryland (
1998 )
Electra pilosa 5/10* Prouho ( 1892 )
6/−* Calvet ( 1900 )
>20/−* Bonnevie ( 1907 )
10–20/17 Up to 80.0 Marcus ( 1926a , b )
440.0 × 360.0 385.0 × 300.0 Atkins ( 1955 )
400.0–500.0
× <400.0
Ryland ( 1965 )
Up to 31/4–15 105.0–178.0 Temkin ( 1996 )
Membranipora serrilamella −/up to 40 100.0 Mawatari ( 1975 )
50.0 (expelled egg) Mawatari and
Mawatari (
1975 )
600.0 × 510.0 Mawatari and Itô (
1972 )
600.0–620.0 ×
480.0
570.0 × 420.0 Mawatari ( 1973a )
−/20–30 85.8–101.0 (width 20.2) Hageman (
1983 )
Membranipora isabelleana 100.0 Cancino et al. (
1991 )
Membranipora tenuis ~25/− Calvet ( 1900 )
Membranipora
membranacea
Up to 40/−* Smitt (
1865 )
−/39 70.0 Silén ( 1945 )
840.0 × 640.0 930.0 × 715 (twinned) Atkins ( 1955 )
−/10–20 (up to
50)
80.0–120.0 × 80.0
(width 30.0)
Eggleston ( 1963 )
750.0–850.0
× 600.0
Ryland ( 1965 )
100.0 Temkin, personal
communication, 2002
−/30 60.0 (expelled egg) Temkin ( 1994 )
Jelliella eburnea 290.0 × 150.0 + 350.0 × 180.0
(twinned)
Taylor and
Monks (
1997 )
Pyripora catenularia 380.0–390.0 × 270.0 Taylor ( 1986a )
In some instances (marked by asterisk) the number of oocytes was determined from published illustrations based on live material total preparations
or anatomical sections; in the latter instance, only oocytes in the section plane could be counted; the size of cyphonautes larvae and ancestrula in
Membranipora serrilamella was determined from illustrations. Symbols: “×”, two longest perpendicular diameters; “–”, range
3 Evolution of Reproductive Patterns in Cheilostomata
235
and metamorphosis, the structures ensuring its autonomous
feeding (capture and digestion of food particles) would have
been no longer needed. The free-swimming period was con-
siderably shortened for the same reason as recorded for lar-
vae of most of the known incubating bryozoans that swim
freely for less than 24 h, in comparison with planktotrophic
larvae that live for periods of 1 week to 2 months (Dudley
1973 ; Yoshioka 1982 ; Cook 1985 ). Also, a reduction of this
period and the evolution of embryonic incubation (which is
compulsory for the development of endotrophic larvae in
bryozoans) might explain the loss of larval protective struc-
tures, that is, the shell of the cyphonautes. Similar changes
have been described in sea urchins, sea stars and brittle stars
(Wray and Raff 1991 ; Byrne 1991a ; Wray 1992 ; McEdward
and Janies 1993 ; Raff 1996 ). A detailed analysis of the loss
of the food- capturing structures in connection with the
acquisition of large oocytes and the transition to a non-feed-
ing larva in some sedentary polychaetes can be found in the
work of Pernet ( 2003 ).
Though our knowledge of bryozoan larvae is incomplete
and fragmentary (reviewed in Barrois 1877 ; Ryland 1974 ,
1976 ; Zimmer and Woollacott 1977a ; Cook 1985 ; Reed
1987 , 1991 ; Mukai et al. 1997 ), we know enough to be able
to say that the class Gymnolaemata, with its broad range of
larval forms, illustrates the above-described hypothetical
sequence of the transition to lecithotrophy. Facultative plank-
totrophic larvae have not been described in Bryozoa, but in
this phylum there are species with lecithotrophic larvae com-
pletely lacking a gut and species whose larvae have a non-
functioning digestive tract reduced to varying degrees.
Non-feeding larvae in three such species in the order
Ctenostomata, i.e. Flustrellidra hispida , Pherusella tubulosa
and P . brevituba , have retained the gut, which is incomplete
posteriorly, and a bivalve shell homologous to that of the
cyphonautes (Zimmer and Woollacott 1977a ). The larva of
the ctenostome Triticella fl ava looks very much like a
cyphonautes but lacks the shell, a mouth and, apparently, an
anus. However, it is the only non-feeding larva to develop a
vestibulum, a body wall invagination characteristic of
cyphonautes larvae. After a short external brooding phase,
the development of such larvae is completed in the plankton,
lasting altogether for a week. According to Ström ( 1969 ),
fully formed larvae further survived in an aquarium for a
month, decreasing in size during this time, indicating that
these larvae use their internal resources (see also Zimmer
and Woollacott 1977a ). In addition, according to Repiachoff
( 1875 , 1878 ) and Ostroumoff ( 1886b ), the coronate larva of
the cheilostome Tendra zostericola has a non-functioning
rudimentary gut, consisting of midgut and rectum (data on
oesophagus and mouth require checking). On the other hand,
the vast majority of bryozoan larvae lack any trace of feeding
and protective structures.
These examples show that the transition from a
planktotrophic to a lecithotrophic larval type is sometimes
accompanied by partial loss of the structures that enable
feeding and protection of the larva, thus illustrating a gradual
transition from one type to another. A rapid transition cannot
be excluded, however. In any case, such a reduction appears
to be expedient only if the larva no longer needs to feed on
its own and has a shorter free-swimming period. According
to the assessment made by Strathmann ( 1978a ) on the basis
of data in the literature, planktotrophy was lost in Bryozoa
three to six times (see also below).
The above facts and arguments are completely at odds with
the hypothesis, suggested by Silén ( 1944 ), that the cyphonautes
larva is of secondary origin. It was based on the assumption
that brood chambers in the phylum are homologous. Silén
thought that the oldest among them was “embryonary”, viz the
internal brood sac of Phylactolaemata, and that the structures
responsible for embryonic incubation in the “Cheilo-
Ctenostomata” evolved from it. Silén thus argued that Recent
bryozoans lacking brood chambers lost the capacity to brood,
which, in turn, resulted in modifi cation of the larva. Silén
postulated that this transition occurred within the Cheilo-
Сtenostomata several times, and that broadcasters evolved
rather late. Recently, Fuchs et al. ( 2011 , p. 11) presented
data on gene-expression patterns indicating “that planktonic
larvae might have secondarily evolved in bryozoans”.
As mentioned in Sect. 2.4.2 , Santagata and Banta ( 1996 ,
p. 178) proposed a hypothesis according to which “vestibular
brooding preceded evolution of ovicells among cheilo-
stomes”. An outcome of vestibular incubation was loss of the
planktotrophic larva. In contrast with my hypothesis, these
authors suggested that extraembryonic nutrition via the
hypertrophied vestibular epithelium was responsible for
enlargement of the embryo and the shift to endotrophy.
Changes in oogenesis were not mentioned. Overall, their
hypothesis was based on misinterpreted facts and assump-
tions and cannot be considered probable (see also Ostrovsky
2002 ; Taylor and McKinney 2002 ; Ostrovsky et al. 2006 ).
Although planktotrophy in invertebrates does seem to
have evolved secondarily in a number of cases (see McHugh
and Rouse
1998 ; Collin 2004 ; Collin et al. 2007 ), data on the
evolution of brooding and reproductive patterns in cheilo-
stome bryozoans, as well as the sequence in which the major
clades appeared in the fossil record, render Silén’s hypothe-
sis as purely speculative and based on assumptions not facts.
Reproductive pattern I is indeed the rarest among Bryozoa.
However, suborder Malacostegina in which it occurs is
the oldest cheilostome clade, and the morphology of the
cyphonautes larva corresponds to the structure of the trocho-
phore, considered to be the initial larval morphotype in many
groups of marine invertebrates (Cori 1941 ; Jägersten 1972 ;
Strathmann 1978a ; Ivanova-Kazas 1986 ). The presence of a
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
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 gymnolae-
mates they are formed on the anal side as noted by Silén
( 1944 ) (see also Jebram 1973 ). That is, these brood cham-
bers 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 accumula-
tion 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 nec-
essarily 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, phoro-
nids 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 opis-
thobranch 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 nutri-
ents allocated for reproduction is stable, then the evolution-
ary 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 dur-
ing 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 gym-
nolaemate 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 repro-
ductive pattern is uncertain (see above), cheilostome broad-
casters 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
237
Continuous egg production possibly explains the fact that
Temkin did not notice polypide recycling in M . membrana-
cea . To sum up, in malacostegines, one fertile zooid during
the reproductive season may produce several tens and even
hundreds of small zygotes about 50–60 μm in diameter that
further develop into planktotrophic larvae.
The situation is very similar in ctenostome broadcasters
in which the number of ovarian and ovulated oocytes
(25–91 μm in diameter) in one zooid at a given time varies
from 6–10 to up to 60 in different species (6–30 in
Hypophorella expansa , about 20 in Victorella pavida ,
Alcyonidium albidum , A . mytili and A . nodosum , from 9–15
to 45 in Farrella repens , up to 60 in Аlcyonidium sp. and A .
fl abelliforme ) (van Beneden
1844 ; Joliet 1877 ; Ehlers
1876 ; Prouho 1892 ; Calvet 1900 ; Marcus 1926a ; Braem
1951 ; Cadman and Ryland 1996 ; Temkin 1996 ; Ryland
2001 ; see also Sect. 3.4.4 and Table 3.2 ). In A . condylocine-
reum , A . epispiculum and A . cellarioides up to 15 ovarian
oocytes are seen in single section plane (Porter and
Hayward
2004 ). Exceptions are A . hydrocoalitum and
Victorella pseudoarachnidia in which zooids with seven
(Porter 2004 ) and four (Jebram and Everitt 1982 ) ovarian
oocytes were subsequently illustrated. However, the num-
ber of eggs is not mentioned in the texts, so this information
has to be checked. Noticeably, in some of the broadcasting
ctenostomes mentioned ( H . expansa , V . pavida , F . repens ,
A . albidum and Аlcyonidium sp.), ovulated oocytes have an
irregular shape, similar to that in broadcasting electrid
cheilostomes.
Thus, both cheilostome and ctenostome broadcasters
show a range in oocyte production, with maximal numbers
of 50–60 eggs and minimal numbers not exceeding 10 per
zooid at a given time. Egg diameter in both instances is
mostly less than 100 μm (always in ctenostomes).
The number of oocytes produced by most gymnolaemate
brooders is usually less and their diameter is larger than in
broadcasters although the correlation is not strict. For instance,
among 22 species of Ctenostomata for which such data are
available in the literature, 11 species produce 10 eggs or less
per zooid (mostly 3–5) and their diameter varies from 70 to
370 μm (see Table 3.2 ). Five species produce 11–16 eggs of
90–340 μm. Six species produce 20 oocytes ( Tanganella
muelleri , Potsiella erecta , see Braem 1951 ; Smith et al. 2003 )
or more: 60 in Triticella fl ava (Ström 1969 ), about 40 in
Paludicella articulata (according to the illustration of Allman
1856 ), about 90 in Nolella dilatata (depicted by Calvet 1900 ),
and more than a 100 in Labiostomella gisleni (see Silén 1944 ),
and oocyte diameter here ranges from 65 to 160 μm in diam-
eter. It should be noted here that the latter species was initially
described as a “protocheilostome” but later was accommo-
dated among ancient ctenostomes (Todd 2000 ). Its method of
brooding, inferred from Silén’s ( 1944 ) anatomical sections,
supports such placement.
Those species that produce maximal numbers of oocytes
have the smallest eggs (65 μm in T . fl ava , 70 μm in L . gisleni )
and those producing the largest eggs (200–350 μm in
Bowerbankia gracilis and 370 μm in Alcyonidium disci-
forme ) form just 1–4 of them. On the other hand, there are
species with an egg diameter of 70 μm that produce 5–6
oocytes ( Panolicella nutans ), and others with an egg diame-
ter of 110 μm ( Paludicella articulata ) and 160 μm ( Pottsiella
erecta ) that respectively produce up to 20 and more than 40.
Thus, in half the ctenostome brooders their oocytes are
larger than in broadcasters (more than 100 μm) although
their numbers can be either small (2–3) or large (up to 20). In
the remainder of the brooding species mature oocyte diame-
ter is comparable with that in broadcasters and egg number
varies from 4–5 to 100 (Table 3.2 ). Since the duration of
embryogenesis in ctenostomes is, like in cheilostomes, 1.5–2
weeks on average (Reed
1988 , 1991 ), the total number of
eggs formed by an ovary throughout the reproductive period
should potentially vary from several tens to hundreds.
However, it should be stressed that, except for Triticella fl ava
which can simultaneously brood up to 20 embryos (Ström
1969 ), in all of these cases the number of ovarian oocytes is
much greater than the number of incubated embryos, and
thus oogenesis is excessive.
To sum up, there is a large overlap in the number and size
of oocytes between ctenostome brooders and broadcasters,
perhaps indicating an evolutionary connection between these
reproductive patterns. Despite acquired embryonic incuba-
tion, some brooding species still produce a large number of
ovarian eggs (comparable with or even exceeding that in
broadcasters) most of which will never be brooded,
however.
In brooding cheilostomes with reproductive patterns II
and IV, 1–3 oocyte doublets (or 2–6 oocytes including nurse
cells) are usually simultaneously present in the ovary (75%
of all species studied). From 7 to 12 oocyte doublets were
found in the ovaries of cribrimorphs, a paraphyletic clade
(probably not monophyletic) with plesiomorphic features.
Margaretta barbata , a more advanced form, is the only spe-
cies to have up to 25 oocyte doublets in the ovary simultane-
ously, which is comparable to the number of oocytes in
broadcasting bryozoans. As only one embryo at a time is
incubated in the peristomial ovicells of Margaretta (see
Waters 1907 ), the reason for such a large number of oocytes
remains obscure, similar to the situation in the above-
mentioned ctenostome brooders.
Thus, the productivity of the maternal zooid is limited by
the carrying capacity of the brood chamber (Silén 1945 ).
There are, in fact, a few cheilostome species (genera
Scruparia , Tendra , Thalamoporella , Macropora ,
Monoporella ) in which several embryos occur in the brood
cavity at the same time, contrary to most cheilostome
brooders. It is possible, therefore, that the total number of
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
238
Table 3.2 The main parameters of oogenesis and brooding in species of Ctenostomata (based on literature data)
Broadcasters
Species
Number of oocytes
(ovarian + ovulated)
Size of mature ovarian
oocyte (μm) References
Alcyonidium fl abelliforme >60 Porter and Hayward (
2004 )
Alcyonidium sp. Up to 60 (ovulated oocytes – up
to 15 – have irregular shape)
91.0 Temkin ( 1996 )
Alcyonidium australe Many small eggs Porter and Hayward (
2004 )
Hypophorella expansa Up to 30 64.0 Ehlers ( 1876 )
5 + 2 (ovulated oocytes have
irregular shape)
Prouho ( 1892 )
6 Prenant and Bobin (
1956 )
Alcyonidium mytili 14* Silbermann ( 1906 )
Up to 20 <80.0 Cadman and Ryland (
1996 )
Alcyonidium nodosum 20 ~60.0 Ryland ( 2001 )
Victorella pavida ~20 Kraepelin ( 1887 )
Up to 19 (5–6 ripe) (ovulated
oocytes have irregular shape)
40.0 Braem ( 1951 )
Alcyonidium albidum 18 + 3 (ovulated oocytes have
irregular shape)
Prouho ( 1892 )
Farrella repens 9–18 van Beneden ( 1844 )
~45 (8 ripe) Joliet (
1877 )
2–10 ripe (ovulated oocytes have
irregular shape)
25.0 Marcus ( 1926a , b )
Alcyonidium condylocinereum 15* 18.0 (early) Porter ( 2004 )
Alcyonidium epispiculum ~15* 15.0 (early) Porter and Hayward (
2004 )
Alcyonidium cellarioides 9–10* (ovulated oocytes have
irregular shape)
Calvet ( 1900 )
Alcyonidium hydrocoalitum 7* 24.0 (early) Porter ( 2004 )
Victorella pseudoarachnidia >4 50.0 Jebram and Everitt ( 1982 )
Cryptoarachnidium argilla (broadcaster?) 5–6 30.0 Banta ( 1967 )
Brooders
Species
Number of oocytes
(ovarian + ovulated) and
incubated embryos
Size of mature ovarian
oocyte or embryo
(μm) References
Labiostomella gisleni >100 (about 10 ovulated eggs of
irregular shape)
70.0 Silén ( 1944 )
1 embryo (matrotrophy)
Nolela dilatata >90 (many tens)* Calvet (
1900 )
1–3 embryos (matrotrophy) Prouho (
1892 )
Triticella fl ava Up to 60 ovulated 65.0 Ström (
1969 )
2–20 embryos
Paludicella articulata ~43 Allman ( 1856 )
4 + 4 Kraepelin ( 1887 )
1 embryo 140.0 × 80.0 Braem ( 1896 )
Potsiella erecta >20 (4 ripe) (+1–2 embryos) 160.0 Smith et al. (
2003 )
Alcyonidium duplex 7–11 Prouho ( 1892 )
6–8 embryos
3–7 embryos ~100.0 Prenant and Bobin (
1956 )
4 (+3 embryos)
11 (+4 embryos)
Tanganella muelleri 5 (+3 embryos) 80.0–90.0 Braem ( 1951 )
10 (+2 embryos)
19 (+1 embryo)
Tanganella appendiculata ~13 (+3 embryos) 95.0 Jebram and Everitt (
1982 )
Up to 6 embryos
(continued)
3 Evolution of Reproductive Patterns in Cheilostomata
239
eggs produced in the ovary of these bryozoans may be gener-
ally higher than in those that brood a single larva at a time.
Nevertheless, additional research is needed to test this
suggestion.
The reduction in the number of offspring is most pro-
nounced in representatives of the family Epistomiidae. In
Synnotum sp. (as aegyptiacum ) and Epistomia bursaria the
female zooid forms a single larva, although the total number
of germinal cells formed in the ovary is presumably greater
(Marcus 1941b ; Dyrynda and King 1982 ). So, taking into
account the limited reproductive season (from 2–3 to several
months for most species), the duration of brooding (10–14
days on the average) and the fact that, with rare exceptions,
only one embryo is incubated in the brood chamber, we may
conclude that in the lifetime of a single ovary one fertile
zooid in Cheilostomata can potentially produce from four to
Brooders
Species
Number of oocytes
(ovarian + ovulated) and
incubated embryos
Size of mature ovarian
oocyte or embryo
(μm) References
Alcyonidium eightsi ? 290.0 × 340.0 Porter and Hayward ( 2004 )
6–12 embryos
Alcyonidium hirsutum >10 Hayward ( 1983 )
4–12 150.0–200.0 Owrid and Ryland ( 1991 )
4–11 embryos
Bulbella abscondita 10–11 (+3 embryos) 90.0–100.0 Braem ( 1951 )
4–6 embryos 100.0 Jebram and Everitt (
1982 )
Alcyonidium diaphanum 6–10 130.0 Chrétien ( 1958 )
4–5 embryos
3* 71.0 × 43.0 (early) Porter ( 2004 )
Alcyonidium polyoum ? 50.0 (early?) Matricon ( 1963 )
4–6 embryos
Panolicella nutans 5 + 1 (+2 embryos) 70.0 Jebram ( 1985 )
2–5 embryos
Flustrellidra hispida 4–5 Prouho ( 1892 )
4–5 120.0 × 75.0 Pace ( 1906 )
4–5 embryos (matrotrophy)
Up to 8 embryos Hayward (
1985 )
Bowerbankia gracilis 2–5 (0–1 ripe) * 80.0 Braem (
1951 )
3 (+1 embryo)*
1–2 (+several young oocytes) 160.0 Reed (
1987 , 1988 , 1991 )
1 embryo 200.0 × 150.0 (larva)
1–4 200.0–352.0 Temkin ( 1996 )
Bowerbankia imbricata 2 Joliet ( 1877 )
1 embryo
Bowerbankia pustulosa 2* Calvet ( 1900 )
1 embryo
Spathipora comma 3 (+1 embryo) 108.0 × 80.0 Bobin and Prenant (
1954 )
1 embryo 69.0 Soule ( 1950a )
Walkeria uwa 2–3 Joliet ( 1877 )
1 embryo (matrotrophy)
Zoobotryon verticillatum 2 Zirpolo ( 1933 )
1 embryo (matrotrophy)
Bantariella cookae ? Banta ( 1968 )
1 embryo (matrotrophy) 20.0 (young)
230.0 × 115.0 (mature)
Alcyonidium disciforme ? Kuklinski and Porter
(
2004 )
1 embryo 330.0–370.0
For many species, the number and size of oocytes were determined from published illustrations (often schematic) based on live material, total
preparations or anatomical sections. In the latter instance (marked by asterisk) only oocytes in the section plane could be counted. Symbols: “×”,
two longest perpendicular diameters; “–”, size or number range
Table 3.2 (continued)
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
240
a dozen larvae. For instance, in the cheilostome Celleporella
hyalina , a single female zooid subsequently brooded four
larvae during 76 days of observations before its senescence
(Hughes 1987 ). Corrêa ( 1948 ) noted that fertile zooids of
Bugula foliolata (as B . fl abellata ) produce three larvae on
average (i.e. during the reproductive season). The same is
probably true of most brooding Ctenostomata.
Considering oocyte size, in the vast majority of cheilo-
stome brooders (66 species studied with patterns II and IV)
oocyte diameter is larger than in broadcasters, ranging from
100 to 400 μm, while 32 species have eggs of 160 μm and
larger. Only eight species have oocytes smaller than 90 μm
(see Sect.
1.2.4 and Table 1.6 ). Thus, when comparing broad-
casters (pattern I) with brooders (patterns II and IV), one can
see a clear bias towards a decrease in the number of oocytes,
accompanied by their enlargement in Cheilostomata. This
trend also exists in ctenostomes, but the correlation between
oocyte size and number is not so strict (see also Sect. 3.4.4 ).
The data presented here for oocyte size/number in gym-
nolaemate bryozoans with contrasting patterns of sexual
reproduction can be considered as evidence of gradual rather
than abrupt changes in oogenesis during transition from
broadcasting to brooding. Although the limited capacity of
brood chambers restricts larval production, several brooders
still produce large numbers of oocytes. Why such a situation
is still relatively common among the Ctenostomata is unclear
since such large oocyte production is clearly redundant in
brooders. It is rare in Cheilostomata, however, most of which
form a small number of large oocytes.
In addition it can be said that oocytes that become richer
in yolk might stay longer in the ovary. In broadcasting mala-
costegines maintained in experimental culture, the develop-
ment of oocytes in the ovary took less time, on average, than
oogenesis in brooding species (Silén 1945 , 1966 ; Dyrynda
and King 1983 ; Temkin, M.H., 2002, personal communica-
tion). So, it seems that the change in oogenesis resulted in a
decrease in the number of oocytes, which became larger and
took longer to form than in broadcasters.
3.1.2.2 Transition to Sequential Maturation
of Oocytes
In broadcasting bryozoans oocytes develop, reach maturity
and ovulate in cohorts (Hageman 1983 ; Temkin 1996 ). In
contrast, in most brooders oocytes mature, ovulate and are
moved to the brood chamber sequentially. Thus, the change
in oogenesis mode (decrease in egg number, increase in egg
size) and the transition from reproductive pattern I to pattern
II were also accompanied by sequential egg maturation.
Silén ( 1945 ) wrote that the emergence and development
rate of the new oocytes in the ovary of Callopora dumerilii
directly depends on the development rate of the leading
oocyte doublet. Thus, the presence of this physiologically
very active cell pair appears to slow down or even block the
division of oogonia and the growth of younger doublets in
the ovary. Besides, it seems that considerable limitations on
the number of simultaneously produced eggs are imposed by
the carrying capacity of the brood chamber: almost all chei-
lostomes incubate one embryo at a time (see above).
The developing ovary in a young zooid contains, as a rule,
a few oogonia, which divide to form primary oocytes. In
brooding cheilostomes from one to several oocyte doublets
are formed in a young ovary in the early stages of oogenesis,
entering the phase of previtellogenic growth sequentially. It
is unknown whether this sequence is associated with the age
of the doublets, but it may be suggested that the older the
doublet and the larger its cells, the more likely it is to lead
the sequence and to continue to grow at a higher rate than
the others. This may be directly associated with its size: the
greater the surface area and the volume of the female cell the
more substances can be transported into and synthesized in
it. Such a doublet might block the accumulation of nutrients
in younger oocytes (those that appear later) as well as mito-
ses in oogonia (for instance, by hormonal regulation). The
leading oocyte doublet may be compared to a powerful
pump channelling the transport of nutrients in the ovary.
After the ovulation of the leading doublet its place is occu-
pied by the second largest (and possibly the second oldest)
doublet. It may be also assumed that for some time following
ovulation the conditions in the ovary become favourable for
new oogonial divisions.
The fi nding in the ovaries of at least 18 brooding cheilo-
stomes of two or more (up to six in Quadriscutella papillata )
vitellogenic (i.e. growing) doublets, indicates that oogenesis
with sequential formation of oocytes originated from the
more ancient variant of oogenesis with simultaneous forma-
tion of several oocytes. In Eurystomella foraminigera and
Bostrychopora dentata all doublets in the ovary (up to three)
are vitellogenic. Further, in both these species yolk granules
are contained not only in oocytes but also in nurse cells.
This indicates that, initially, nutrient reserves accumulate in
both siblings (see below). The fact that in some species
( Nematofl ustra fl abellata , Isosecurifl ustra angusta ,
Columnella magna ) a pair of vitellogenic doublets at early
stages develops more or less synchronously is reminiscent of
oogenesis in broadcasters (Hageman 1983 ) and, thus, may
indicate the connection between reproductive patterns I and
II. It is only somewhat later that development becomes asyn-
chronous, with one of the doublets considerably outstripping
the other.
The only known ctenostome brooder with numerous ovu-
lated oocytes is Triticella fl ava , which externally broods
numerous embryos. Small cohorts of simultaneously devel-
oping eggs are recorded in those ctenostome brooders that
simultaneously incubate one or several embryos. In contrast,
in the majority of species with only one embryo incubated at
a given time, oocyte development, maturation and ovulation
3 Evolution of Reproductive Patterns in Cheilostomata
241
are sequential. Additional to the above discussion on egg
size and numbers, the available data on simultaneous oocyte
development can be considered as further support for sce-
narios illustrating the main trends in the hypothetical transi-
tion between the two patterns.
3.1.2.3 Shorter Duration of Larval Development
The change in the mode of oogenesis and the transition to a
new larval type resulted in considerable modifi cation of
embryonic development. There were also corresponding
changes in genome activity (Wray and Raff 1991 ; Raff 1996 ).
A mathematical model describing reproduction in marine
invertebrates (Vance 1973 ) establishes a correlation between
productivity (increasing with decreasing egg size) and mor-
tality (depending on the life span of the larva). The model is
based on the assumption that egg enlargement results in (1)
an increase in the length of the prefeeding period, and (2) a
reduction in the feeding period. Speaking generally, egg size
(i.e. amount of nutrients stored in the oocyte) can infl uence
the larval life span by affecting its duration (see also above).
Though Vance’s model does not take into account numerous
factors that may infl uence development rate (for instance
temperature; see Hoegh- Guldberg and Pearse 1995 ), it is nev-
ertheless a plausible refl ection of the situation observed in
nature (Strathmann 1977 , 1985 ; Havenhand 1995 ; Marshall
and Bolton 2007 ). To note, the mathematical model by
Havenhand ( 1993 ) indicates that reduction of the larval devel-
opment period provides a selective advantage.
Does the increase in the size of oocytes indeed infl uence
the duration of larval development? Researchers are divided
on this point. On the one hand, a considerable body of evi-
dence indicates a correlation between larval type and the
duration of the development period from egg to juvenile –
the life span of planktotrophic larvae to competency is typi-
cally longer than lecithotrophic ones that usually develop
from larger eggs (Todd and Doyle 1981 ; Emlet et al. 1987 ;
Wray and Raff 1991 ; Havenhand 1993 ; Hoegh-Guldberg and
Pearse
1995 ; Raff 1996 ). So it is generally thought that the
larger the eggs, the shorter the development. The idea behind
this is that the nutritive reserves contained in the oocyte fuel
the acceleration of development and metamorphosis
(Villinski et al.
2002 ) through higher physiological rates and
heterochronies (Raff 1996 ). This dependence has been
described, for instance, for sea urchins, and it is often quite
well expressed even if we compare species with planktotro-
phic larvae developing from eggs of different size (Sinervo
and McEdward 1988 ; Wray and Raff 1991 ; Hoegh-Guldberg
and Pearse 1995 ). When comparing development time from
fertilization till metamorphosis in two species of Clypeaster
(Echinoidea) with planktotrophic and facultative-
planktotrophic larvae correspondingly, it was 9 days less for
the species with the larger eggs and facultative planktotrophy
(Emlet
1986 ). Experiments with isolated blastomeres of two
other species from the genus Strongylocentrotus demon-
strated a negative correlation between blastomere diameter
and the rate of development at early embryogenesis stages:
the smaller the initial blastomere, the slower the develop-
ment rate (after a certain size has been achieved, the rate of
development is restored) (Sinervo and McEdward 1988 ).
On the other hand, an analysis by Underwood (
1974 )
demonstrated the absence of any such correlation in proso-
branch molluscs, some insects and birds. Ghiselin ( 1987 ),
too, in his review cited data from Spight ( 1975 ) about the
decreasing development rates with increasing size of oocytes
in gastropods, i.e. the tendency appears to be just the oppo-
site (see also Emlet et al. 1987 ; Havenhand 1993 ; Hoegh-
Guldberg and Pearse 1995 ; Marshall and Bolton 2007 ). For
instance, the development of the planktotrophic larva of the
sea star Porania antarctica is completed two weeks faster
than the lecithotrophic larva of Porania sp. At the same time,
the diameter of oocytes in these two co-occurring species is
the same (Bosch 1989 ). Strathmann ( 1977 ), too, reported
both variants from different groups of marine invertebrates.
After comparing the data in the literature, Hoegh-
Guldberg and Pearse ( 1995 ) came to the conclusion that the
key factor determining the rate (and duration) of develop-
ment of echinoderm larvae is water temperature [To note,
Clarke ( 1982 , 1992 ) considered this factor to be unimportant
for the development rate of invertebrates in polar waters].
The comparison made by the two above-mentioned authors
showed that, despite the slower development rates of plank-
totrophic larvae (given the same temperature) as compared
with lecithotrophic ones, a correlation between oocyte diam-
eter and the duration of development is not at all obvious.
Against the background of a distinct dependence between
the larger size of oocytes and the shortened duration of
development, numerous contradictory examples stand out –
among echinoderms there are both species with small
oocytes and rapidly developing planktotrophic larvae and
species with large oocytes and slowly developing lecithotro-
phic larvae. So, as with the correlation between oocyte size
and larval type (see above), it is probable that the depen-
dence under discussion does exist but is not as distinct as
generally thought.
As for bryozoans, the life span of cyphonautes larvae
(which are formed from microlecithal eggs) varies from pre-
sumably a few days (Dudley 1973 ) to 2 months (Marcus
1926b ; Kluge 1975 ) in different species. Indeed, larvae of
the malacostegine Membranipora membranacea reportedly
live 4 weeks in the sea, and survived up to 8 weeks in the
laboratory (Yoshioka 1982 ). Cadman and Ryland ( 1996 ),
having compared the dates of the reproductive peak in the
ctenostome broadcaster Alcyonidium mytili and the peak of
occurrence of its cyphonautes larvae in the plankton, con-
cluded that the life span of these larvae should be 4–6 weeks.
Planktonic larval duration is not known for Electra , although
3.1 Modifi cation of Oogenesis and Its Evolutionary Consequences
242
assumed to be similar (Saunders and Metaxas 2010 ). The
long development of the cyphonautes larva may be explained,
among other things, by irregular food supply and by the fact
that some of the acquired energy is spent on feeding and
locomotion. In contrast, species of the malacostegine genus
Conopeum appear to have relatively short-lived planktotro-
phic larvae with a lifespan of a few days only (see Cook
1962 ; Dudley 1973 ). Dudley suggested that there is a trend
towards “reduction” of planktotrophic larva in the malaco-
stegine genera Membranipora , Electra and Conopeum . The
largest and longest-living cyphonautes larvae are formed in
Membranipora , and the smallest ones, with the shortest life,
in Conopeum . Since egg size in malacostegines (and broad-
casting ctenostomes) is fairly similar (being normally less
than 100 μm diameter, see Tables 3.1 and 3.2 ), it is clearly
does not affect the duration of larval life.
Theoretically, the increase in the amount of nutrients
transferred to the oocyte by the parent organism should result
in a shorter duration of development. If the nutritional
reserves are suffi cient to cover all needs to reach a competent
state and pass through metamorphosis, then feeding is not
required, and the duration of the larval period can be short-
ened. Indeed, on average, bryozoan endotrophic larvae
(formed from macrolecithal eggs) develop faster than
cyphonautes larvae, but again this is not very strict.
The developmental period of non-feeding bryozoan lar-
vae consists of the incubation period during which
embryogenesis takes place and a free-swimming period
until larval settlement. In the laboratory, the latter period in
most bryozoan species studied is several hours to 1 day.
Only in a few species can large larvae swim for up to 4–5
days (Cook 1985 ). For the entire larval developmental
period until metamorphosis, an extreme example comes
from the descriptions of Paltschikova-Ostroumowa ( 1926 )
and Braiko ( 1967 ), who reported that embryogenesis in the
brood chamber of the cheilostome Tendra zostericola takes
from 10 h to 2 days. After that, according to observations in
the laboratory, the larva spends from 6–8 h to 2 days in the
water column before settlement. Thus the period from ovi-
position to metamorphosis takes from 16 h to 4 days. It
should be stressed here that the diameter of oocytes in this
species is only 70 μm (Braiko 1967 ), which is comparable
to the size of oocytes in cheilostomes with planktotrophic
larvae. Thus, the egg size being similar, development in
Tendra occurs faster than even in those gymnolaemate
broadcasters whose larvae have the shortest life (about a
week presumed for Conopeum , see above). A similar situa-
tion occurs in the ctenostome brooder Triticella fl ava whose
larvae develop from oocytes 65 μm in diameter during
approximately 8 days (Ström
1969 ). In addition, the small
egg size in these two species shows that premetamorphic
development is energetically not very costly (see also Byrne
et al. 2003 ).
Further comparison is hampered because of the very large
range of larval-development time (1–8 weeks) in broadcast-
ers that all have small eggs of about the same size. Another
obstacle is the scarcity of data on the duration of larval devel-
opment. In general, most gymnolaemate brooders have
larger eggs than broadcasters and their lecithotrophic larvae
develop faster than the longest-living planktotrophic larvae
(10–14 days vs 1–2 months in Electra and Membranipora ).
At the same time, the duration of development in brooders is
comparable to or possibly longer than that in short-lived
cyphonautes larvae (in Conopeum ). For instance, non-
feeding larvae of the ctenostome Bowerbankia gracilis
develop from eggs 350 μm in diameter in 12–14 days (Reed
1988 , 1991 ). According to Nielsen ( 1981 ), larval develop-
ment in Pacifi cincola insculpta (egg diameter 250 × 225 μm)
took about the same time, i.e. 11–15 days in the sea and 6–15
days in the laboratory. In Fenestrulina miramara (as mea-
sured from the illustration, egg diameter is 320 × 270 μm),
larval development took 10–14 and 10–13 days, respectively,
under the same conditions. Interestingly, Silén ( 1945 )
reported that development of the larva of the cheilostome
Callopora dumerilii from a much smaller oocyte (120 μm in
diameter) also took two weeks (under laboratory conditions).
Thus from comparing developmental time in brooders, one
can conclude that, (1) larvae from eggs of strongly differing
size can take the same time to develop, and (2) larvae from
larger eggs ( Pacifi cincola , Fenestrulina ) can develop faster
than larvae from smaller eggs ( Callopora ). The latter conclu-
sion accords with the suggestion that a reduction in develop-
ment time may be correlated with egg enlargement. However,
the situation can be opposite, too, since development takes
just 8 days in T . fl ava (egg diameter 65 μm) and 12–14 days
in B . gracilis (350 μm). Also, the wide variation in larval
development time in Pacifi cincola insculpta should be noted.
At the same time, in some cheilostome species the dura-
tion of development of endotrophic larvae is comparable
with that of long-lived cyphonautes larvae. For instance,
brooded larvae of Cryptosula pallasiana in Nova Scotia
were developing in the aquarium for approximately 30
days (Gordon 1977 ) (oocyte diameter 180 × 150 μm, pers.
obs.). It is unclear whether this time corresponds to the
duration of larval development in nature, however. A simi-
lar duration has been reported for larvae of the matrotro-
phic brooder Celleporella hyalina , which take 3–4 weeks
to develop in natural conditions in north Wales (Cancino
and Hughes 1988 ) (oocyte diameter about 80 μm) although
the developmental time can be shorter, just 12–14 days
(Hughes 1987 ). The same egg size (80 μm) is characteris-
tic of the matrotrophic cheilostome Bugula foliolata (as
B . fl abellata ), whose larva develops over two weeks (see
Corrêa 1948 ), and it seems that extraembryonic nutrition
does not increase larval developmental time, at least on
some occasions.
3 Evolution of Reproductive Patterns in Cheilostomata
243
Thus, although a general correlated trend in the reduction
of development time with egg enlargement seems to exist in
gymnolaemate bryozoans, the situation is less than straight-
forward, being strongly complicated by the large variation in
egg size and duration of development in both brooders and
broadcasters.
Interestingly, the above facts show that the shortest
embryogenesis among brooding gymnolaemates is
observed in the species with the least-derived reproductive
traits, including small numerous oocytes and primitive
brooding modes, that is, in the cheilostome Tendra zosteri-
cola and the ctenostome Triticella fl ava . In more advanced
gymnolaemates with larger oocytes or with relatively small
oocytes and matrotrophy, embryogenesis is noticeably lon-
ger. Also, the fully formed larvae of Triticella , which have
a body shape reminiscent of cyphonautes larvae and a non-
functioning gut, reportedly lived in the aquarium for a fur-
ther month, gradually becoming smaller (Ström
1969 ).
Similar examples are known among asteroids with leci-
thotrophic larvae (discussed in Emlet et al. 1987 ). It is
unclear if this ability for prolonged starvation is an
advanced trait connected with accumulation of extra
reserves in the egg, or a primitive character state inherited
from a cyphonautes larval form adapted to a non-stable
food supply.
The examples of Tendra and Triticella indicate the possi-
bility of the following scenario. In the evolution of gym-
nolaemate bryozoans, the duration of embryogenesis was at
fi rst considerably reduced following the transition to
lecithotrophy owing to an accumulation of additional nutri-
ents in the oocytes. One may suggest that the fi rst lecithotro-
phic larvae with a rudimentary gut, resembling those of
Tendra and Triticella , developed from small oocytes (similar
in size to the oocytes of the ancestors with planktotrophic
larvae). Since these larvae did not have to feed, they achieved
a competent state much faster than did cyphonautes larvae.
Later in evolution, however, oocytes increased in size by
accumulating additional nutrients and this was accompanied
by secondary prolongation of the duration of endotrophic
larval development. As a result, there are species with leci-
thotrophic larvae and prolonged development (e.g.
Cryptosula pallasiana ), comparable with that of long-lived
planktotrophic larvae.
Hoegh-Guldberg and Pearse ( 1995 ) suggested that, given
the same temperature and food availability for planktotro-
phic larvae, the latter would develop at approximately the
same rate as lecithotrophic ones owing to the general depen-
dence of metabolic rates on water temperature. The authors
concluded that any kind of feeding (acquisition of food or the
use of the already-available resources) does not signifi cantly
infl uence the evolution of development rates. As a critical
remark, it can be said that while rates of development of exo-
and endotrophic larvae are probably similar, their periods of
development are usually quite different (see above). A plank-
totrophic larva not only acquires energy during feeding but
also spends it on food capture and locomotion. Throughout
their (often quite long) life span, such larvae spend up to half
of their total energy on food acquisition, which may be irreg-
ular (Hoegh-Guldberg and Emlet 1997 ). Lecithotrophic lar-
vae are entirely “carefree” in this respect and could accelerate
their development, in particular, by means of heterochronies,
“skipping” certain (usually, early) stages of embryogenesis
and reaching a competent state faster (Raff
1996 ). It should
be noted that Hoegh-Guldberg and Emlet ( 1997 ) demon-
strated experimentally a higher level and rates of metabolic
activity in lecithotrophic larvae as compared to planktotro-
phic ones in Heliocidaris sea urchins.
3.1.2.4 Changes in Ovary Structure
All gymnolaemates are characterized by a common basic
plan of organisation of the female gonad (Reed
1991 ; pers.
obs.), its variants (see Chap. 1 ) presumably refl ecting the
stages of evolution of this organ. Evolutionary changes in
oogenesis would inevitably have been accompanied by
changes in gonad structure. Compared to species with repro-
ductive pattern I, those with patterns II and IV have a more
compact ovary and a more distinct intraovarian zone, which
corresponds to the sequential formation of a few large gam-
etes. The compact ovary of bryozoans with patterns III and V
(Dyrynda and King 1982 ) consists of a few cells and has a
barely discernible intraovarian zone. Such a structure results
from the formation of a few oligo- or mesolecithal eggs in
these ovaries. Therefore, the difference in the structure of the
female gonad in species with different reproductive patterns
may be explained by the difference in the mode of gamete
production. This was fi rst noticed by Waters ( 1912 , 1913 ; see
Sect. 1.3.3 ), who categorised ovaries of different species into
two groups based on oocyte size and number. Although not
describing (but illustrating) ovarian structure itself, Waters
correctly noted that ovaries contain 2–3 small oocytes in
bugulids (pattern III), whereas many eggs, one of which
reached a considerable size, were seen in the candids studied
(pattern II).
3.2 Early Fertilization and Origin
of Nurse Cells
The relationship between sperm morphology and the cir-
cumstances of fertilization have been broadly discussed
(Franzén 1956 ; Kasyanov 1989 ; Ryland and Bishop 1993 ;
Drozdov and Ivankov 2000 ). The sperm of all three classes
of bryozoans are considered to be highly modifi ed compared
to the primitive sperm of animal groups with external fertil-
ization (Franzén 1956 , 1970 , 1987 ; Woollacott 1999 ), indi-
cating that internal fertilization emerged early in the evolution
3.2 Early Fertilization and Origin of Nurse Cells
244
of bryozoans, possibly increasing the probability of contact
between male and female gametes.
The type of reproduction when only sperm is released into
the environment and enters female individuals or zooids is
referred to as spermcast mating (Bishop and Pemberton
2006 ). In spite of the apparent very high risk of sperm mortal-
ity, fertilization success in gymnolaemate bryozoans is very
high too, varying from 83 to 100% (Temkin
1994 , 1996 ; Yund
and McCartney 1994 ; Bishop and Pemberton 2006 ).
Moreover, all of the bryozoans studied, including stenolae-
mates and phylactolaemates, have intraovarian fertilization.
In the broadcasters studied (two malacostegines and a cteno-
stome), fertilization occurs immediately before or during
ovulation (Temkin 1994 , 1996 ). In the brooding ctenostome
Boverbankia gracilis , sperm penetrates the mature macroleci-
thal oocyte located in the ovary (Temkin 1996 ), whereas in
Nolella stipata and Alcyonidium sp. sperm was found in the
ovary in “growing” oocytes (developmental stage not indi-
cated) (Marcus 1938 ). Thus, it seems that in brooding cteno-
stomes fertilization occurs in the ovary, apparently at a rather
late stage of oocyte development. In contrast, Chrétien ( 1958 )
wrote that in A . diaphanum polypide degeneration begins
before vitellogenesis starts, i.e. the alien sperm should be
obtained by a zooid during much earlier stages of the oogen-
esis. Similarly, in all the brooding cheilostomes studied, early
oocytes are fertilized (see Sect. 1.3.6 ).
So, one may suggest that the evolution of fertilization in
Gymnolaemata proceeded towards earlier fusion of male and
female gametes. “Ovulatory” fertilization (during ovulation
or immediately after it) became intraovarian (Ostrovsky
2008 , 2009 ). This shift may be perceived to enhance sperm
survival – spermatozoids probably could live longer by
entering the ovary. Moreover, in this instance of sperm stor-
age the zooid, having once obtained sperm, no longer
depends on an additional fertilization event.
Why or how cheilostomes acquired very early (preco-
cious) fertilization of early primary oocytes is unclear (see
Sect.
1.3.6 ). It may have been a side effect of the evolution
of internal fertilization itself, ensuring the meeting of gam-
etes in small immobile epibionts. Sperm succeeding in
entering the ovary began to fuse with very young oocytes.
Important consequences of early fertilization would have
been (1) the development of oocytes in pairs (oocyte doublets)
and (2) dependence of the inception of vitellogenesis upon
fertilization.
In Membranipora membranacea , the division of the
oogonium results in a pair of early primary oocytes that
remain connected by a cytoplasmic bridge for some time
(Hageman
1983 ). If the earliest brooding cheilostomes had
had the same feature, then the transition to precocious intra-
ovarian fertilization and fusion of one of two young oocytes
(still connected by a cytoplasmic bridge) with the male gam-
ete could have prevented the completion of cytokinesis.
Syngamy typically triggers a cortical reaction that trans-
forms a vitelline membrane into a fertilization envelope. In
the case of an oocyte doublet, such an envelope should form
around both cells since their membranes are still continuous
(Ostrovsky 2008 ). Detachment of the fertilization envelope
from the oolemma is delayed, however, and this may prevent
young oocytes from completing cytokinesis. Thus, siblings
are forced to stay together, further differentiating into the
vitellogenic oocyte and its nurse cell. A detailed ultrastruc-
tural study of early oocyte doublets would shed light on this
problem. For instance, Dyrynda and King ( 1983 , p. 475)
recorded what they called “the precursor of the vitelline
envelope” or “primary coat” around both the oocyte and its
nurse cell during early vitellogenesis in two cheilostome
brooders. Further evidence in support of the idea that nurse
cells originated as a result of early fertilization is their
absence in broadcasting cheilostomes and brooding cteno-
stomes, which appear to lack early fertilization (but see
example of A . diaphanum in Chrétien 1958 ).
A rather curious observation was made by Marcus ( 1941a )
who wrote that in Thalamoporella evelinae the nurse cell fi rst
fuses with the oocyte and then fertilization occurs. This infor-
mation should be verifi ed but if it is true it means that repro-
ductive pattern II emerged in Thalamoporella independently,
as did its ovicells. Marcus ( 1934 ) also described and illus-
trated what he called “nurse cells” in the phylactolaemate
Lophopus crystallinus . He considered them abortive oocytes
but in his illustrations the cell pairs consisting of an oocyte
and a “nurse cell” closely resemble oocyte doublets in cheilo-
stomes. It is unfortunately not known if these cells are real
siblings or if there is a cytoplasmic bridge between them.
The presence of nurse cells in the viviparous Epistomiidae
remains unclear. If the so-called “follicle” cells surrounding
the oocyte (Dyrynda and King 1982 ) are not nurse cells but
cells of the ovary wall, then nurse cells could have been lost
in this family, and the single oocyte is formed from a single
oogonium. If the “follicle” is of germ-cell origin then the
nurse cells substitute an ovary. Gordon (
2012 ) placed
Epistomiidae near Beaniidae in his classifi cation, and incu-
bation in the latter family occurs in internal brood sacs. If
epistomiids are indeed related to beaniids, they may have
lost brood chambers when they became viviparous.
Specialization of the nurse cells in Cheilostomata was
related to the change in their synthesizing activity. Yolk
granules in the cytoplasm of the nurse cells have been found
in about 30 bryozoan species (see Table
1.7 ). Their presence
may indicate that in the early stages of evolution of the new
reproductive pattern nurse cells functioned identically to
oocytes, forming a nutrient reserve (yolk), but it is unclear if
this reserve was transported to the sibling. Later, nurse cells
in most species began to produce mostly RNA, presumably
transporting it to the sibling’s cytoplasm across the cytoplas-
mic bridge (see Dyrynda and King
1983 ). Hypertrophied
3 Evolution of Reproductive Patterns in Cheilostomata
245
development of the nucleus is one of the main arguments in
this connection. For example, in Porella minuta and P . smitti ,
mature nurse cells have a very large nucleus occupying most
of the cell, with the cytoplasm looking like a narrow periph-
eral ring. Large nuclei indicate that these cells actively pro-
duce RNA, although their cytoplasm also contains yolk
granules. This example may represent an intermediate evolu-
tionary stage from the ancient variant (the nurse cell predom-
inantly producing yolk) to the advanced variant (the nurse
cell forming ribosomes). Other species possibly illustrating
this trend are Hippoporina reticulatopunctata and Bugulopsis
monotrypa , in which mature nurse cells do not contain yolk
granules whereas the nurse cells of early vitellogenic oocytes
do, as if the early stages of nurse-cell functioning recapitu-
lated the ancient form of synthesis and the later stages the
advanced one.
3.3 Evolution of Matrotrophic Incubation
in Cheilostomata
3.3.1 Origin of Placentotrophy
In contrast to most other invertebrate phyla, extraembryonic
nutrition (EEN) is common in Bryozoa (Levin and Bridges
1995 ; Batygina et al. 2006 ; Ostrovsky et al. 2009a ; Lidgard
et al. 2012 ). All matrotrophic bryozoans are equipped with
temporary structure(s) that, together with the apposed part of
the embryo, act as a “simplifi ed placenta-like system”
(Woollacott and Zimmer 1972a , b ; 1975 ). EEN is thought to
be obligatory in living stenolaemates and phylactolaemates
(Reed 1991 ; Mukai et al. 1997 ; Ostrovsky 2009 ), relatively
widespread in Cheilostomata (Ostrovsky et al. 2008a , 2009a )
and, as recently shown at the ultrastructural level, present in
Ctenostomata (Ostrovsky and Schwaha 2011 ).
In discussing bryozoan reproductive strategies, Nielsen
( 1990 ) emphasized that as well as the three major patterns
there are also several “intermediate types”, alluding to the
total diversity of bryozoan reproductive variants. In the
event, this terminology is applicable – the recently discov-
ered pattern IV is an intermediate variant between reproduc-
tive patterns II and III (Ostrovsky et al. 2009a ). Following
the terminology of Kasyanov ( 1989 ), there was a transition
from a lecithotrophic embryonic strategy to a placental one.
Insofar as the numbering terminology of reproductive pat-
terns I to III has become established in the literature the
newly discovered pattern had to be assigned IV, but this is
not intended to refl ect the evolutionary sequence.
Although cheilostomes with reproductive patterns I and III
share the feature of yolk-poor oocytes, their oogenesis differs
considerably, indicating that pattern III is unlikely to have
evolved from pattern I. For instance, it would be hard to
explain the great difference in the number of oocytes
formed by species with these patterns during oogenesis.
Paleontological data also do not support the idea that species
with pattern III evolved from an ancestor with pattern I. In
contrast, the type, size and number of oocytes in bryozoans
with patterns II and IV are similar, indicating the essential
similarity, if not identity, of their oogenesis types. In addition,
species with these patterns may have more than one vitello-
genic doublet in the ovary; further, these patterns are found
within the same genera and families. All these facts support
the idea that pattern IV evolved on the basis of pattern II via
acquisition of the placental analogue, further transforming to
pattern III (Ostrovsky et al. 2009a ; Ostrovsky 2013 ).
A recently proposed scenario describing the main steps of
the advent of placentotrophy in cheilostome bryozoans sug-
gested that the evolution of the new reproductive patterns
proceeded as a cascade of events including transitions from
reproductive pattern I to pattern II, from pattern II to pattern
IV, and further from pattern IV to pattern III (Ostrovsky et al.
2009a ; Ostrovsky 2013 ). These transitions involved two cor-
responding shifts in oogenesis from oligo- to macrolecithal
(during transition from pattern I to II) and back (from pattern
IV to III). The latter shift could have been triggered by the
acquisition of placentotrophy during incubation, which grad-
ually substituted ovarian vitellogenesis as a major source of
the nutrients needed for embryonic development. An inverse
correlation between the degree of maternal provisioning
during oogenesis and matrotrophic gestation is well-known
among invertebrates and vertebrates. For instance, less-yolky
eggs are known to develop in echinoderms possessing EEN
(Byrne 1991b ; Wray 1995a ; Byrne and Cerra 1996 ; Byrne
et al. 1999 ). Greatly reduced vitelline systems are character-
istic of some matrotrophic monogenean fl atworms (Cable
and Tinsley 1991 ). Such reduction is considered to be an
evolutionary trend in matrotrophic cestodes (Swiderski and
Xylander 2000 ; Korneva 2005 and references therein) and
the same trend can be also inferred from the data on egg
types in scorpions (Francke 1982 ) and matrotrophic isopods
(Hoese and Janssen
1989 ). Among vertebrates, some highly
placentotrophic squamate reptiles ovulate eggs with a
reduced egg content (reviewed in Blackburn
1993 ). Finally,
in mammals, the evolution of placentation resulted in a shift
to microlecithal oogenesis based on the loss of the yolk
genes (Rothchild 2003 ; Brawand et al. 2008 ).
Why nutrient transfer during incubation should have
evolved in bryozoans is unclear. One possibility is that ini-
tially it was relatively unimportant and played no role in
embryonic development. The next step could have appeared
in the form of precocious ovulation and oviposition, as a
result of a non-mature egg being transported to the incuba-
tion chamber. In this way, the role of EEN in provisioning
resources to the embryo may have gradually changed from
supplementary to central. This change is likely to have
accompanied a transition from a weakly functioning (or small)
3.3 Evolution of Matrotrophic Incubation in Cheilostomata
246
embryophore to one that was active, and thus from incipient
to substantial placentotrophy. The redistribution of the load
was refl ected in the structure of the ovary – fi rst of all, in the
number and size of its cells. Oocytes gradually became
smaller, accumulated less yolk and began to ripen faster.
A commonly accepted scenario for the evolution of
matrotrophy is based on the development of viviparous ver-
tebrates (see Packard et al.
1977 ; Blackburn 1992 , 1993 ,
1999a , 2005a , 2006 ). In this case, internal fertilization and
retention of eggs are the major preconditions. Primitive fetal
nutrition would have been strictly lecithotrophic and devel-
oped further by the addition of small quantities of nutrients
from the reproductive tract of the viviparous female. This
so-called “incipient matrotrophy” is considered to have been
an initial step towards the evolution of the “specialized”
(Wourms 1981 ) or “substantial matrotrophy” (Blackburn
1992 ) that was accompanied by a subsequent shift in oogen-
esis. Examples corresponding to this scenario have been
thoroughly studied in squamate reptiles (reviewed in
Blackburn
1992 ) and poeciliid fi shes (Reznick et al. 2002 ;
Pollux et al. 2009 ; reviewed in Wourms 1981 ; Marsh-
Matthews et al. 2010 ). When we deal with placenta-like sys-
tems, the term “incipient placentotrophy” can be applied
(Blackburn 1993 , 2005a , b ).
As for invertebrates, incipient matrotrophy (and some-
times placentotrophy) almost certainly exists among
onychophorans (Anderson 1973 ), scorpions (Farley 2001 )
and insects (Hagan 1951 ), although no defi nitive statements
concerning this phenomenon have been made.
My results indicate that both incipient and substantial
placentotrophy is present among cheilostome bryozoans.
Moreover, the fi nding of different modes of oogenesis and
degrees of embryonic enlargement and embryophore devel-
opment in a variety of species (see Sects. 1.2.5 and 1.2.6 )
gives insight into the scenario(s) of transition from one of
these nutritional modes to the other. Considering cheilo-
stomes with reproductive pattern IV fi rst, small placental
analogues (embryophores) have been recorded in four spe-
cies with large macrolecithal oocytes that are slightly smaller
than the brood cavity or comparable in size to it ( Klugefl ustra
antarctica , Isosecurifl ustra angusta , Micropora notialis and
Figularia fi gularis ). Slight/negligible (ca 1.5-fold) enlarge-
ment of the embryo in them suggests a small nutrient supply.
Ultrastructural or experimental evidence is missing and it is
possible that EEN is absent. Hypertrophy and increase in the
number of embryophore cells together with the change in the
staining of their cytoplasm might then be explained, for
instance, by active gas exchange or/and removal of waste
material from the brood chamber. The most important sign
of a maternal-fetal physiological relationship is a recogniz-
able response of the maternal cells to the appearance of a
zygote in the brood chamber, which points to molecular
transport. Even if EEN is absent, the establishment of such a
relationship can be the basis for further acquisition of
matrotrophy. In passing, it may be noted that mother-to-
embryo nutrient transfer has been recorded in experiments
involving a number of poeciliid teleost fi shes with large
yolky eggs (Marsh-Matthews et al. 2010 ).
In three species ( Cellaria tenuirostris , Cribricellina
cribraria and Watersipora subtorquata ) with the same repro-
ductive pattern (IV), the embryo becomes noticeably larger
(3–3.39-fold increase) in comparison with mature macro-
lecithal eggs, despite hypertrophy of the embryophore cells
in these species being rather modest. Thus, a degree of mor-
phological development of the placental analogue is not nec-
essarily directly correlated with its nutritive activity.
Elaboration of placental structures has been known to corre-
late with a degree of nutritional provisioning during gesta-
tion in teleost fi shes (Turner 1940 ) and some scinks
(Flemming and Blackburn
2003 ), but my data show that it is
not always the case in cheilostomes (Ostrovsky
2013 ).
In six other cheilostomes (pattern IV, Beania bilaminata ,
Bicellariella ciliata , Celleporella hyalina , “ Calyptotheca ”
variolosa , Costaticella solida , C . bicuspis ), embryo enlarge-
ment is substantial or even very substantial and comparable
with that in species with pattern III [Despite the absence of
late embryos in available colonies C . bicuspis , a well-
developed embryophore and the size difference between the
early embryo and the brood cavity allows for the inclusion of
this species here]. Actually, except for differences in mode of
oogenesis (macrolecithal vs oligolecithal), these two repro-
ductive variations are identical, both involving an embryo-
phore with strongly hypertrophied cells and eggs that are
considerably smaller than the brood cavity (Moosburgger
et al. 2012 ; Ostrovsky 2013 ).
Based on this information, it might be suggested that a
combination of large macrolecithal oocytes comparable in
size to that of the brood cavity, and minimal embryonic
enlargement provided by a small embryophore corresponds to
the earliest stage in the evolution of placentotrophic incuba-
tion (incipient placentotrophy). Species with macrolecithal
oocytes (smaller than the brood cavity), a functionally active
embryophore and substantial embryonic increase could exem-
plify the next step, representing an intermediate stage in the
evolution of placentotrophy. My data show that such species in
Bryozoa exhibit the entire range of egg sizes from large (more
than 300 μm in Cribricellina cribraria ) to tiny (about 50 μm
in Beania bilaminata ) along with embryophore development,
thus demonstrating a decrease in the size of macrolecithal
oocytes, a corresponding decrease in ovarian activity and,
oppositely, an increase in placental activity. Thus, a shift from
incipient to substantial matrotrophy/placentotrophy occurred
in species with macrolecithal oogenesis. Until now, such
variation in maternal provisioning and placental structure has
been recorded only in squamate reptiles (Stewart 1992 ;
Blackburn
1993 , 1999a ; Stewart and Thompson 2000 ) and
3 Evolution of Reproductive Patterns in Cheilostomata
247
some teleost fi shes (Turner 1940 ; Wourms 1981 ; Reznick
et al.
2002 , 2007a ; Marsh-Matthews et al. 2010 ).
The fi nal step in this hypothetical transition from pattern
IV to pattern III was a shift from the production of small
macrolecithal to meso- or oligolecithal eggs, supported by
substantial placentotrophy. Among species with pattern III,
maximum embryonic enlargement was recorded in those
with the smallest oocytes ( Bugula neritina , Reciprocus rega-
lis , Mollia multijuncta , Pterocella scutella ), and it is in these
species that the difference between egg size and brood-cavity
size was most prominent.
As in pattern IV, species with pattern III demonstrate dif-
ferent degrees of embryo enlargement and embryophore
development. There is no clear correlation between these two
characters, however, and species with both strong and modest
hypertrophy of the cells of the placental analogue demon-
strate a wide variation in embryo enlargement. For instance,
species with modest hypertrophy of embryophore cells
showed a range of enlargement from 4.9-fold in C . tenuiros-
tris to 53.4 in Mollia multijuncta , as did species with strong
hypertrophy of these cells: from 6.3-fold in Bugula fl abellata
to 310-fold in B . neritina . Thus, as in pattern IV, two variants
of substantial placentation – with modest and strong hyper-
trophy of placental-analogue cells – are detectable among
species producing eggs with a small amount of yolk.
The specifi c case of Myriapora truncata , which combines
large macrolecithal eggs and strong hypertrophy of the
embryophore cells (pattern IV), is puzzling. Its zygote occu-
pies the entire cavity of the ovicell so that further embryonic
growth should be strongly restricted. This case may be an
example of rapid evolution of a well-developed placental
analogue, contrasting with the model of gradual acquisition
of the embryophore as discussed above. Another possible
explanation is that in Myriapora truncata the embryophore
serves exclusively for excretory purposes, removing wastes
produced by the large embryo (Ostrovsky 2013 ).
3.3.1.1 Critical Remarks
Conclusions about incipient matrotrophy in bryozoans can
be criticized because of the lack of data on intraspecifi c
(intracolonial, seasonal, geographic) variation in embryo-
phore development and larval size in the species in which
inferred EEN is responsible for embryo “increase”. Working
on living material, Cancino and Hughes ( 1988 ), Wendt
( 2000 ), Marshall et al. ( 2003 ), Marshall and Keough ( 2003 ,
2004a , 2006 , 2008a , b) and Kosman and Pernet ( 2009 )
showed that larval size can vary or be rather stable within and
between populations of the same species. All of the species
studied are matrotrophic brooders belonging to the genera
Celleporella , Bugula and Watersipora , some with small, others
with substantial increase in embryo size during incubation.
It is not clear why larval size varies in these taxa, however.
In Bugula neritina , larvae increase with parent- colony wet
mass (Marshall et al.
2003 ), at higher colony densities
(Marshall and Keough
2008b ) and in colonies following
toxicant exposure (Marshall 2008 ), and diminish in experi-
mentally halved colonies (Marshall and Keough
2004b ),
thus being supposedly dependant on colony state (see also
Marshall and Keough 2009 ). If egg size is stable then
recorded variations in larval size would refl ect variation in
the EEN, i.e. the placenta is a means by which the colony
controls larval size. Such functional fl exibility of bryozoan
placental analogues may point to an evolutionary past in
which their progressive modifi cation led to the acquisition of
substantial matrotrophy. In fact, Bugula neritina demon-
strates the largest larval increase during brooding ever
recorded in cheilostomes.
It is important to note that no research was carried out on
the egg size variation in the afore-mentioned studies; thus it
is not known if (and how) this trait might infl uence variation
in larval size. Evidence for such a connection would consid-
erably add to our understanding of variability in larval size.
In my fi xed material, the maximum size of both mature
oocytes and late embryos was stable although the sample
size was low compared with the studies mentioned above,
and volume estimation using histological sections is clearly
not as precise as the methods used by the above authors. It is
clear that larger sample sizes are required to increase the sta-
tistical power of embryo-enlargement analyses. However,
multiplication of embryophore cells, their hypertrophy and
cytological change as well as discrepancy in size between
the mature egg and brood cavity and changes in embryonic
yolk content all point to the existence of EEN. Even if the
increase in embryo size is small and nutrient transfer is neg-
ligible, the morphological evidence strongly supports the
inference that some exchange (more than just of gases and
water) occurs between the embryo and the parent.
Another factor to consider is that of water absorption as a
reason for embryo enlargement. In studies on vertebrates,
measurements of changes in dry mass are currently the main
indicator of EEN whereas volume and wet mass are not con-
sidered as reliable criteria (Blackburn
1994 ). One reason is
that developing embryos always increase in wet mass and
volume (due to water uptake), regardless of whether matrot-
rophy is present.
In contrast with vertebrates, embryonic size increase is
still widely used as evidence of matrotrophy in invertebrates
and lower chordates. Experiments with radiolabelling and
diet manipulation (Toolson 1985 ; Hoese and Janssen 1989 ;
Frick 1998 ) as well as ultrastructural studies (Domenici and
Gremigni 1977 ; Cable and Tinsley 1991 ; Schwartz and
Dimock 2001 ; Korneva 2005 ) are very rare. Instead many
authors have recorded and described anatomical changes in
both the parent and the offspring during incubation, considering
such changes as additional evidence for matrotrophy (e.g.
Hagan
1951 ; Mukai et al. 1987 ; Farley 2001 ; etc.). The small
3.3 Evolution of Matrotrophic Incubation in Cheilostomata
248
size of eggs and embryos is the main obstacle for using dry
mass in studies of matrotrophy in most invertebrates; the only
study that used such data dealt with a terrestrial isopod
(Lawlor 1976 ). The same obstacle pertains to bryozoans. In
this phylum, apart from ultrastructural evidence (see above),
embryo enlargement during incubation, together with accom-
panying morphological changes in the embryophore and the
embryo, are currently the main criteria used to ascertain the
occurrence of EEN. Water uptake is obviously a useful crite-
rion but the degree to which it takes place is unknown. It may
be noted that some increase in embryo volume was recorded
in a number of non-matrotrophic cheilostome brooders. In the
vast majority it ranged from 1.05 to 1.3-fold, reached 2.5-fold
in a few species (see Table
1.8 ). Such an increase is compa-
rable with that recorded in species with presumed incipient
matrotrophy, but there were neither a developed embryophore
nor detectable changes in embryo cells to provide evidence of
nutrient transfer in the former species, suggesting water
uptake in them (see also Ostrovsky 2013 ).
3.3.2 Multiple Origins of Placentotrophy
in Cheilostomata
Matrotrophy and, in particular, placentotrophy are generally
regarded as having evolved many times in different classes
of vertebrates (Wourms 1981 ; Blackburn et al. 1985 ;
Blackburn 1992 , 1999b , 2005a ; Wooding and Burton 2008 ).
Similarly, the distribution of the patterns of sexual reproduc-
tion across Bryozoa strongly suggests that placentotrophy
evolved independently in all three bryozoan classes and
within both gymnolaemate orders (Ostrovsky et al. 2009a ).
Unfortunately, a robust phylogenetic framework is still lack-
ing for Bryozoa. Published molecular phylogenies are very
incomplete (at best analysing species from less than 10% of
all described genera) and contradictory in many important
details (see Tsyganov-Bodounov et al. 2009 ; Fuchs et al.
2009 ; Knight et al. 2011 ; Waeschenbach et al. 2012 ). As for
matrotrophic cheilostomes, only a few species from the
matrotrophic genera Bugula , Beania , Watersipora and
Cellaria as well as Bicellariella ciliata and Celleporella hya-
lina were involved in the molecular analysis, and in all pub-
lished phylogenetic trees the distribution of matrotrophic
taxa is very patchy. Species of Bugula and Beania are situ-
ated within the same branch in the trees made by Knight
et al. (
2011 ), and Bicellariella ciliata is placed in the same
branch with Bugula in the tree by Tsyganov-Bodounov et al.
( 2009 ). Such a placement implies the possibility of a com-
mon ancestor with EEN for some lineages within Buguloidea
but a more rigorous analysis of the superfamily is required,
involving many more taxa.
One of the major arguments in favour of this suggestion
for Cheilostomata is the presence of two, or sometimes three,
patterns of sexual reproduction in the same families and the
presence of two patterns in the same genera. In other words,
in many instances closely related species can be matrotrophic
or non-matrotrophic, or, if matrotrophic, may have different
modes of oogenesis. Species with pattern II (non-matrotro-
phic with macrolecithal oogenesis) and pattern IV (matrotro-
phic with macrolecithal oogenesis) have been recorded in the
families Candidae, Cribrilinidae and Hippothoidae. Patterns
II, III (matrotrophic with microlecithal oogenesis) and IV are
known in Bugulidae, Flustridae, Cellariidae and, apparently,
Catenicellidae. Two different patterns have been found in
Gregarinidra (II and III), Isosecurifl ustra (II and IV) and
Microporidae and Cellaria (III and IV) (Ostrovsky et al.
2009a ; Ostrovsky 2013 ). A similar situation has been
described in teleost fi shes of the families Poeciliidae and
Zenarchopteridae, in which close relatives “vary either in a
presence or absence of matrotrophy or in the degree to which
matrotrophy is developed” (Reznick et al. 2002 , 2007a , p.
2570). To note, the molecular analysis showed that matrotro-
phy may have evolved independently not only within these
families but also within several different genera (Reznick
et al. 2002 , 2007a ; Pollux et al. 2009 ; Pires et al. 2011 ;
Meredith et al. 2011 ).
The cheilostome genus Bugula is notable for having vari-
ous degrees of matrotrophy resulting in embryo enlargement
from 6.3- to 500-fold in different species (Woollacott and
Zimmer 1975 ; Dyrynda and King 1983 ; pers. obs.). This
attribute is reminiscent of the continuum of variation in
matrotrophic provisioning recorded in such fi sh genera as
Poeciliopsis , Nomorhamphus and Dermogenys (see Reznick
et al. 2002 , 2007a ). Variation in the degree of EEN has been
suggested among populations of the poeciliid fi sh Phalloceros
caudimaculatus (see Arias and Reznick 2000 ).
Intraspecifi c variation among oocyte types and larval
increase during matrotrophic incubation were detected in
distant populations of Bugula fl abellata . Dyrynda and King
( 1983 , p. 489) described “telolecithal” (= macrolecithal) eggs
77 μm in diameter in the Irish Sea colonies that had larval size
150 μm. My material from New Zealand contained oligoleci-
thal eggs (96 × 55 μm) and larvae 160 × 120 μm in diameter.
Even if these populations are represented by different (but
clearly very closely related) species, the presence of two
different modes of oogenesis may point to the shift between
patterns IV and III within this clade (Ostrovsky 2013 ).
3.3.3 Plausibility of an Alternative Scenario
The proposed sequence of events in the evolution of placen-
totrophy within cheilostome bryozoans may be questioned
by making a case for reversibility of matrotrophy. An alter-
native scenario would then be that EEN originated in a hypo-
thetical early brooder producing relatively small mesolecithal
3 Evolution of Reproductive Patterns in Cheilostomata
249
eggs (a hypothetical ancient variant of pattern II, resulting in
a non-feeding larva, see Sect.
3.4.1 ). Further evolution could
result in a transition from incipient to substantial placentot-
rophy with corresponding enlargement of both the embryo
and the brood chamber (pattern III). The transition to macro-
lecithal oogenesis accompanied (or not) by the enlargement
of oocytes could lead to pattern IV and ultimately to the sup-
pression of matrotrophy, which could then fi nally disappear
through a shift to pattern II.
However, this alternative scenario is made doubtful by
two major arguments: the pattern of EEN distribution among
the taxa and the timing of their appearance in the fossil
record. First of all, though EEN has turned out to be com-
moner among Cheilostomata than previously thought, the
majority of them are still non-placental. It seems extremely
unlikely that matrotrophy evolved in the ancestral brooder,
became widespread and then was lost many times in differ-
ent families. For instance, only one supposedly matrotrophic
Recent species ( Crassimarginatella falcata ) is known among
Calloporidae (Cook 1985 ), the earliest brooding family
known since the Albian (Late Cretaceous) and considered as
ancestral to a number of cheilostome lineages, including
microporids and cribrilinids. Yet the genus Crassimarginatella
itself is much younger, having evolved in the Danian (Early
Paleocene). There are similar additional examples in the
families Microporidae, Cribrilinidae, Poricellariidae and
Hippothoidae. Originating in the Late Cretaceous
(Cenomanian), the Cribrilinidae and Microporidae are two
other large “key” families supposedly ancestral to many of
the more advanced cheilostome lineages (Boardman et al.
1983 ; Gordon and Voigt 1996 ; Gordon 2000 ). In the
Microporidae, which probably evolved from a calloporid
ancestor, only two Recent species ( Micropora notialis and
Mollia multijuncta ) are known to possess EEN. Whereas
Micropora is known from the Cenomanian, Mollia is much
younger, having evolved in the Danian. In the largest
cheilostome family, Cribrilinidae, matrotrophy is suggested
in just one species ( Figularia fi gularis ), and the genus
does not appear until the Miocene. At the end of the
Cretaceous (Maastrichtian) two other genera – Poricellaria
(Poricellariidae) and Celleporella (Hippothoidae) – evolved
of which three Recent species are matrotrophic.
Secondly, although it is possible that placental analogues
are more widespread than is known for cheilostomes (sexual
reproduction has been studied anatomically in species from
less than 30% of all families), the paucity of matrotrophic
representatives among Recent genera of basal clades and the
large gaps between their time of origination suggest that pla-
cental analogues are unlikely to have evolved early and to
have achieved wide distribution in the Cretaceous.
Interestingly, the number of genera with proven or suggested
EEN increases considerably in the Tertiary. Eight genera
belonging to eight families are known since the Eocene
( Scrupocellaria , Beania , Cellaria , Figularia , Catenicella ,
Adeonellopsis , Hippopodina , Myriapora ), six other
genera from four families since the Miocene ( Costaticella ,
Adeonella , Laminopora , Synnotum , Watersipora , Urceo-
lipora ), and one genus from the Oligocene ( Pterocella ). Nine
genera from fi ve families have no fossil record, i.e. they
either evolved relatively recently ( Retifl ustra , Isosecurifl ustra ,
Gregarinidra , Klugefl ustra , Bugula , Bicellariella , Epistomia ,
Cribricellina , Reciprocus ) or simply have not yet been dis-
covered in the fossil record (in some cases because they are
lightly calcifi ed). It seems that matrotrophy was becoming
more and more common during cheilostome history, but again,
phylogenetic relationships between taxa including matrotro-
phic species, together with the distribution of reproductive
patterns, point to its independent origins (Ostrovsky 2013 ).
As a fi nal remark, in squamate reptiles, live-bearing (and,
subsequently, matrotrophy) was much more easily gained
than lost (Lee and Shine 1998 ), whereas in teleost fi shes
there is no evidence of such transitions (Goodwin et al. 2002 ;
Mank et al. 2005 ). Although hypotheses about reversals are
actively discussed, most authors tend to consider the acquisi-
tion of this novelty as a dominant trend in comparison to its
loss (Wourms and Lombardi 1992 ; Shine and Lee 1999 ;
Blackburn 1999c ; Reznick et al. 2007b ; Pollux et al. 2009 ;
see also Blackburn 2005a , b ). On the other hand, the mater-
nal input can be highly labile. For instance, Dulvy and
Reynolds’s ( 1997 ) phylogenetic analysis showed 6-8 rever-
sals from matrotrophic to lecithotrophic viviparity in elas-
mobranchs (see also Reynolds et al. 2002 ). Thus, estimates
of the number of independent origins of matrotrophy should
be combined with phylogenetic character mapping.
3.3.4 Origin of Viviparity in the Family
Epistomiidae
An exceptional case of independent evolution of EEN is rep-
resented by the viviparous family Epistomiidae, which pos-
sesses intraovarian matrotrophic incubation (reproductive
pattern V). In this group the origin of matrotrophy might
have been associated with the transition from incubation of
embryos in the brood chamber (for instance, in the internal
brood sac, as in Beaniidae) to embryonic development
directly in the ovary.
According to Dyrynda and King ( 1982 ), the “epis-
tomiid” character state – intracoelomic incubation (larval
viviparity) and absence of polypide recycling – is the initial
variant, the basis for the subsequent evolution of extracoe-
lomic brooding accompanied by degeneration-regeneration
of polypides. Their line of argument is clear – non-brood-
ing ancestral forms with one polypide generation in the
zooid gave rise to the species with intracoelomic incubation
and no recycling and then extracoelomic brooding appeared.
3.3 Evolution of Matrotrophic Incubation in Cheilostomata
250
The development of the embryo outside the maternal zooid
allowed polypide regeneration, while spatial separation of
gametogenesis and brooding allowed multiple use of the
fertile zooid.
To begin with, this hypothesis is not supported by paleon-
tological data – brooding in ovicells dates back to the Middle
Cretaceous whereas the fi rst epistomiids ( Synnotum ) are
known from Miocene deposits. Epistomiids have avicularia
similar to those of bugulids so their ancestor probably
belonged to the same superfamily (Buguloidea) possessing
extrazooidal brooding. Sexual dimorphism characteristic of
the Epistomiidae is also a derived character. Further, it is dif-
fi cult to imagine a reason for the transition from viviparity
(generally considered as derived and an evolutionarily expe-
dient form of parental care) to external brooding involving
egg transfer from the zooid. Any kind of internal brooding
ensures good protection of the embryo and the possibility of
forming a large larva. So even if epistomiids did originate
from a non-brooding ancestor, this was a cul-de-sac branch
in the evolution of brooding.
This family is much more likely to have evolved from
bryozoans with extrazooidal brooding (pattern II) by acquir-
ing intrazooidal/intraovarian embryonic incubation. As with
the above-discussed transition from pattern IV to pattern III,
the mode of oogenesis shifted from macrolecithal to
microlecithal.
3.3.5 Adaptive Importance of Placental
Analogues in Cheilostomata
If, as argued above, placental analogues indeed evolved
numerous times (at least, 22) in bryozoans, the question
arises about the selective importance of such a feature.
Existing hypotheses reasonably consider placentation as a
byproduct of the evolution of parental care in Cheilostomata.
Santagata and Banta ( 1996 , р. 178) proposed a hypothesis,
according to which the earliest form of embryo incubation
was “vestibular brooding,” which resulted in the acquisition
of placental nutrition via the vestibular wall (see above).
Another hypothesis was suggested by Hughes ( 1987 ),
who thought that skeletal brood chambers initially were pro-
tective structures, later assuming the function of extraembry-
onic nutrition in some species. The structure of different
types of brood chambers, their distribution among cheilo-
stomes as well as fossil evidence all point in favour of this
hypothesis.
Dyrynda and Ryland ( 1982 ), who described polypide
recycling in the maternal zooid during matrotrophic brood-
ing in Bugula fl abellata , suggested that the “evolution of
embryonic placentation” (p. 255) provided an uninterrupted
nutrient supply to the embryo during periods when the feed-
ing apparatus and gut (polypide) degenerated, thus support-
ing maximum larval production in bryozoans with ephemeral
colonies. However, in matrotrophic Beania bilaminata and
Watersipora subtorquata , and in all catenicellids and urceo-
liporids studied so far, the polypide never regenerates during
placentotrophic incubation. The same is true of species in the
family Epistomiidae (see above), in which uninterrupted
EEN is supported by intracolonial transport of nutrients via
funicular cords (Marcus 1941b ; Dyrynda 1981 ; Dyrynda and
King 1982 ). Thus, as with oogenesis, matrotrophic nutrition
occurs independently of the presence or absence of a func-
tioning polypide (see Dyrynda and Ryland 1982 ; Dyrynda
and King 1983 ; Ostrovsky 1998c , 2009 ). This suggests a
high degree of colonial integration, enabling interzooidal
distribution of nutrients to non-feeding (including incubat-
ing) zooids. Thus, any connection between the evolution of
placentotrophy and polypide recycling is unlikely.
The role of EEN in accelerating embryogenesis, though
possible, is unknown. For instance, in matrotrophic
Celleporella hyalina the larva is incubated from 12–14 days
(Hughes 1987 ) to 3–4 weeks (Cancino and Hughes 1988 ).
Similarly larval development requires from 10–14 to 30 days
in non-matrotrophic cheilostomes studied (see Silén 1945 ;
Gordon 1977 ; Nielsen 1981 ). So, at present the data are too
few to draw fi rm conclusions.
It was suggested earlier that EEN affords simultaneous
embryonic development and growth and thus may acceler-
ate the rate of reproduction in the early part of the process
(Ostrovsky et al. 2009a ). The fi rst small microlecithal oocyte
in the ovary of species with pattern III should theoretically
mature faster than the large macrolecithal egg in non-
placental brooders with pattern II. While the macrolecithal
oocyte is maturing, the microlecithal oocyte will be trans-
ferred to the ovicell, and the new egg will begin its forma-
tion in the ovary immediately after oviposition. In this
situation, the speed of embryogenesis would not be impor-
tant. Of more importance is that the fi rst larvae will be
released earlier in matrotrophs since their oogenesis is
shorter. For instance, it takes about 4 weeks from the begin-
ning of egg formation in the ovary until larval release in
Callopora dumerilii (Silén 1945 ) and 6 weeks in Chartella
papyracea (both non- matrotrophic cheilostomes) and just
3 weeks in matrotrophic Bugula fl abellata (Dyrynda and
Ryland 1982 ; Dyrynda and King 1983 ) and B . simplex
(Grave 1930 ; Ryland 1974 ). Mawatari ( 1951 ) found that B .
neritina released its fi rst larvae just 1 week after the fi rst few
ovicells were observed in the colony. Such a strategy (simul-
taneous embryonic growth and development) would benefi t
species with ephemeral colonies that live in seasonal waters,
allowing them to occupy free biotopes/niches because of
more rapid production of the fi rst generation of larvae.
Indeed, matrotrophy has been recorded in the families
Bugulidae, Beaniidae, Candidae, Flustridae, Cellariidae,
Poricellariidae, Catenicellidae, Urceoliporidae and
Epistomiidae, the species of which all possess erect weakly
calcifi ed colonies and many evidently live just a few months.
3 Evolution of Reproductive Patterns in Cheilostomata
251
Brief colony life is also characteristic of the hippothoid
Celleporella hyalina (Eggleston
1972 ). These observations
are in accord with recently discussed data on poeciliid fi shes
in which placentation is associated with an increase in the
rate of production of offspring early in life (Pires et al.
2011 ). However, many cheilostome species with ephemeral
colonies have no embryophore (Ostrovsky
1998c , 2009 ,
2013 ; Ostrovsky et al. 2009a ; Moosburgger et al. 2012 ) and
there are some matrotrophic species with long-lived, heav-
ily calcifi ed colonies (e.g. Myriapora truncata , species of
Adeonidae and some other families).
3.3.6 Prerequisites and Role of Embryo
in Evolution of Matrotrophy
The origin of EEN in Cheilostomata became possible only
after complete isolation of the incubatory space from the
external medium. This condition was also considered to be
indispensable for the evolution of matrotrophy in bivalves
(see Richard et al.
1991 ). Another prerequisite was the per-
meability of at least part of the wall of the brood chamber to
low-molecular substances, allowing their bidirectional
transport.
In the experiments of Silén ( 1945 ), embryos of the non-
matrotrophic cheilostome Callopora dumerilii rapidly died
after being transferred from ovicells to sea water. Thus, the
fl uid in the brood chamber, the cavity of which is topologi-
cally exterior, appears to be considerably different from sea-
water, being probably chemically infl uenced by the maternal
zooid via the non-calcifi ed wall of the ooecial vesicle.
Osmoregulatory and excretory relationships involve
active maintenance of the periembryonic environment via
physiological mechanisms during incubation (Lombardi
1998 ). The developing embryo is metabolically active, and
one can speculate that the transport of small molecules
occurs in both directions (for instance, simple sugars and
amino acids from the coelomic fl uid of the fertile zooid to the
brood chamber and excretory metabolites from the fl uid of
the brood cavity back to the visceral coelom). This may have
initially been a passive mechanism, driven by concentration
gradients together with gas exchange. Since hypertrophy of
the embryophore cells in matrotrophic bryozoans occurs
only when the embryo is in the brood chamber, it is likely
that a direct chemical infl uence (signal) causes changes in
the embryophore cells, stimulating their hypertrophy. One
may speculate that their increased size and activity refl ects
an “attempt” to blockade/neutralize the excretory metabo-
lites of the embryo by producing substances that afterwards
became a source of nutrition for it. Even if this is not the
case, it can be assumed that EEN is a by-product of the
chemical relationship between the developing embryo and
its “parent”. On the other hand, the infl uence of the embryo
does not result in the formation of placental analogues in
most cheilostome brooders studied. It is especially intriguing
that both variants have been found in species of the same
genus Catenicella .
3.3.7 Matrotrophy and Evolution of Sexual
Polymorphism in Cheilostomata
It seems that the evolution of matrotrophy could have induced
zooidal sexual polymorphism. Harmer ( 1926 ) suggested that
the change from brooding in ovicells to incubation in an
internal sac “has probably been induced by the supply of an
increased amount of nutrient yolk to the embryo” (p. 254).
Although the transition from external to internal brooding in
some families was probably associated with better embry-
onic protection (see Ostrovsky et al. 2006 , 2007 , 2009b ),
matrotrophic incubation inside a voluminous zooid might
have resulted in additional embryonic enlargement. Thus,
matrotrophy may have facilitated the origin of sexual poly-
morphism since many, if not all, species in the cheilostome
family Adeonidae (presumably entirely placentotrophic) are
characterized by larger orifi cial size and, in many instances,
enlarged brooding zooids. Similarly, EEN might have
resulted in the evolution of polyembryony and enlarged
gonozooids in the bryozoan class Stenolaemata (Ostrovsky
2013 ) and female zooids in Epistomia .
3.3.8 Distribution of Placentotrophy
in Bryozoa
While modes of EEN have been thoroughly reviewed in ver-
tebrates (Wourms 1981 ; Wourms et al. 1988 ; Wourms and
Lombardi 1992 ; Blackburn 1992 , 1999b , 2005b ; Blackburn
et al. 1985 ; Wooding and Burton 2008 ), there has been no
attempt to review the topic in invertebrates. Modes of matrot-
rophy occurring during embryonic incubation include ooph-
agy, adelphophagy, histotrophy, histophagy, and
placento trophy (modifi ed from Wourms 1981 and Blackburn
et al. 1985 ; Blackburn 1999b ). Chordates possess all these
modes, with placentotrophy commonest. It exists in mam-
mals (except monotremes), many squamate reptiles, a rela-
tively large number of bony and cartilaginous fi shes, some
ascidians and all salps (Wourms 1981 ; Mukai et al. 1987 ;
Godeaux 1990 ; Blackburn 1993 ; 2005a , b ; Wooding and
Burton 2008 ). An equivalent variety is found among inverte-
brates, but histotrophy is the commonest mode. Placentotrophy
evolved in Porifera, Cestoda, Scorpiones, Insecta, Gastropoda,
Onychophora, Kamptozoa and Bryozoa (Ereskovsky 2010 ;
Hagan
1951 ; Anderson 1973 ; Tompa 1984 ; Nielsen 1990 ;
Reed
1991 ; Farley 2001 ; Korneva 2005 ), but in most of these
groups there are only a few placental species. In contrast,
scorpions (currently more than 1,700 species) are, appar-
ently, all placentotrophic (Farley 2001 ). “Pseudoplacental
3.3 Evolution of Matrotrophic Incubation in Cheilostomata
252
viviparity” has been recorded in about 800 species of Diptera,
Dermaptera and Psocoptera, and in all aphids (Hemiptera)
(about 4,000 species) (Hagan
1951 ; Meier et al. 1999 ;
Bermingham and Wilkinson
2009 ). Considering the enor-
mous overall number of arthropod species, these fi gures are
perhaps not so surprising. Phylum Bryozoa is much less
numerous (about 6,000 described Recent species), but the
number of species with placental analogues is of the same
order of magnitude. Placental analogues have evolved in all
bryozoan classes, including 87 known species of the freshwa-
ter class Phylactolaemata and about 850 species of Recent
stenolaemates (order Cyclostomata). My calculations, based
inter alia on the assumption that all species of Bugula ,
Watersipora , Adeonidae and Epistomiidae are matrotrophic,
indicate about 175 species for cheilostomes. Ten ctenostome
species also exhibit EEN (reviewed in Ostrovsky et al.
2008a ,
b ; 2009a ). Thus, at least a thousand bryozoan species are
placentotrophs, making this phylum the leader among all
aquatic invertebrates. Based on the distributional pattern of
EEN throughout the phylum, as well as the independent ori-
gin of embryonic incubation, matrotrophy apparently evolved
at least 22 times in Bryozoa.
3.4 Causes, Stages and Consequences
of Transition to Endotrophy
in Cheilostomata and Ctenostomata
Oviparity, external fertilization and planktotrophy are con-
sidered to be primitive characters (Jägersten 1972 ;
Strathmann 1978a , b , 1985 , 1993 ; McHugh and Rouse
1998 ). Among Bryozoa spermcasting, zygote spawning and
planktotrophy are attributes of reproductive pattern I, which
is thus thought to be the most ancient. It is logical to suggest
that the other patterns evolved on this basis, but the precise
causes of their origin remain open to debate.
Evolution of the lecithotrophic larva was most probably a
result of changes in oogenesis: an accumulation of more
nutrients in oocytes brought about a reduction in the larval
gut and numerous other changes. Thus, the new larval type
evolved during transition to the new reproductive pattern II
combining macrolecithal oogenesis and embryonic incuba-
tion. In this section I attempt to reconstruct this sequence of
events, discussing possible preconditions, causes and conse-
quences of the origin and further evolution of new reproduc-
tive patterns in bryozoans.
3.4.1 Lecithotrophy and Brooding
The origin of lecithotrophy in Bryozoa invites a number of
intriguing questions. Why do all living bryozoans with
parental care have lecithotrophic larvae? And, by contrast,
why is there not a single example of a lecithotrophic larva in
broadcasting bryozoans? Lecithotrophic larvae develop from
macrolecithal eggs, so was the evolutionary change in oogen-
esis somehow connected with the origin of embryonic incu-
bation? The origin of brooding and lecithotrophy had
dramatic consequences for phylum Bryozoa but what is the
connection between these two phenomena?
According to the mathematical model of Vance ( 1973 ),
species with numerous offspring and species with a reduced
number of young (in our case, with exo- and endotrophic
larvae) are equally successful (stable) from the evolutionary
viewpoint (see also Chia 1974 ), often coexisting in the same
biotopes. This model compares oocyte size expressed
through the amount of energy in regard to development rate
and mortality rate. According to the improved version of this
model (Christiansen and Fenchel 1979 ), the reproductive
pattern refl ects a compromise between productivity and sur-
vival rate. Prolonged existence in the water column and high
elimination rate of the larvae is compensated for by the large
number of eggs they develop from. On the other hand, a
decrease in the number of offspring should be compensated
for by a shorter free-swimming period, which in turn may be
compensated for by a higher development rate or embryonic
incubation. Data on the development rates of most endotro-
phic larvae of cheilostome bryozoans show that without
brooding they would spend a considerable time in the envi-
ronment, which would result in higher mortality. Obviously,
the role of parental care in the survival of the young is very
important.
An overwhelming majority of invertebrates with leci-
thotrophic larvae brood their young (Wray 1995a ). Chia
( 1974 ) suggested that, owing to energetic constraints, small
invertebrates cannot produce enough eggs to ensure recruit-
ment through dispersal, thus compensating for a small num-
ber of offspring by their larger size. Production of the large
oocytes is correlated with lecithotrophy and parental care
(brooding or viviparity) (see also Jablonski and Lutz 1983 ;
Valentine and Jablonski
1983 ; Olive 1985 ). Although it has
been criticized (Strathmann and Strathmann
1982 ), this
hypothesis remains rather attractive. When both the amount
of resources allocated for reproduction and the capacity of
the ovary are limited, the transition from oligolecithal to
macrolecithal oocytes (and from a planktotrophic to a leci-
thotrophic larva) results in larger size and a smaller quantity
of oocytes. This tendency, however, is fraught with risk. The
relationship between the productivity of an organism and the
survival rate of its offspring is a critical factor (Vance 1973 ;
Christiansen and Fenchel 1979 ; Jablonski and Lutz 1983 ).
Though a reduction in offspring number (accompanied by an
increase in nutrient reserves in each egg) in non- broadcasting
bryozoans may be in some degree compensated by the (1)
numerous reproductive zooids in a colony, (2) larval enlarge-
ment, and/or (3) shortening of larval life, these factors
3 Evolution of Reproductive Patterns in Cheilostomata
253
possibly are not suffi cient to provide a positive balance between
survival and mortality. Theoretically, the consequences of a
decrease in the number of offspring might be compensated by
embryonic incubation, enabling development inside the
maternal organism or in specialized brooding structures. In
both cases, the time spent in the water column, the most
hazardous for the young organism, is drastically shortened.
The suggested connection between incubation and a
decrease in the number of young corresponds to the conclu-
sion made by Smith and Fretwell (
1974 ) – the more energy
(including parental care) is allocated to an offspring, the bet-
ter are its chances for survival (also discussed in Emlen
1973 ; Strathmann 1978b ; Poulin and Féral 1996 ). Moreover,
according to Picken ( 1980 ), a free larval stage is absent in
some species with protected development, since they pro-
duce relatively few ova, and incubation ensures a high level
of offspring survival. A similar correlation between larger
size and smaller number of eggs and parental care was
described in fi shes (discussed in Balon 1991 ).
As for invertebrates, most ophiuroids that brood their
young are characterized by reduced fecundity (Byrne 1991a ).
In this group embryonic incubation supposedly evolved in
relation to the acquisition of larger eggs, non-feeding larvae
and smaller adult size (Byrne 1991a ; Byrne et al. 2008 ).
Considering bivalve mollusks, Sellmer ( 1967 ) wrote that
incubation is an evolutionary adaptation to having a reduced
number of young, which in turn is connected to the small
parental size (see also Mackie 1984 ). Zarenkov ( 1982 ) noted
that the decrease in body size characteristic of the crustacean
subclass Copepoda is associated with reduced productivity,
such species tending to evolve parental care. Incubation and
short-lived larvae are characteristic of many colonial epibi-
otic invertebrates. Notably in ascidians, almost all colonial
species (with smaller zooids) have parental care, whereas
solitary species do not (Strathmann and Strathmann 1982 ;
Strathmann 1990 ). Strathmann ( 1978b , 1990 , 1986 ) explained
the association of brooding with small adult size by the
necessity of a normal oxygen supply to the embryos (see also
Strathmann et al. 1984 ). According to this relationship, since
fecundity increases disproportionally with surface area as
adult size increases, larger animals are less capable of
successfully brooding their offspring.
On the whole, internal incubation, often associated with
viviparity, is usual in groups of small-sized invertebrates
(Levin and Bridges 1995 ; see also the review of hypotheses
in Ghiselin 1987 ). Taking into account the microscopic size
of bryozoans and the relatively small number of oocytes (and
even smaller number of brooded larvae) formed by zooids in
brooding species, the evolution of embryonic incubation
appears to have been an extremely important, possibly cru-
cial, event in bryozoan evolution, allowing them to compen-
sate for the reduction in the numbers of offspring during the
transition from planktotrophy to lecithotrophy.
Finally, when analyzing the hypothesis that is in question
here, Strathmann and Strathmann ( 1982 ) asked why brood-
ing is also not so typical of large animals. Indeed, numerous
small eggs and planktotrophic larvae usually develop in
larger broadcasting species whereas smaller species are nor-
mally brooders producing relatively large eggs and non-
feeding larvae (reviewed in Olive 1985 ). Following the idea
of Chia ( 1974 ), I suggest that non-brooding Echinodermata
with non-feeding larvae compensate for the decrease in the
number of oocytes accompanying the evolution of lecithot-
rophy by the larger size of the maternal individual and thus
by the greater number of gametes it produces. In other words,
for relatively large animals, with their numerous eggs, the
decrease in the number of oocytes associated with an increase
in size is not so risky as it is for smaller animals.
A shift in oogenesis (reduction in egg number and increase
in their size) and parental care can apparently evolve in the
cheilostomes sequentially, with a short time lag. One can
argue that oogenesis becomes modifi ed fi rst, with the
decrease in the number of offspring caused by it compen-
sated soon after by the origin of brooding. Wray ( 1995a ) also
suggested that lecithotrophy preceded the origin of brooding.
Besides, the above-described independent multiple origin of
brood chambers within Cheilostomata (see Chap. 2 ) indi-
cates that the non-feeding larva and thus the new mode of
oogenesis also evolved several times. In my opinion, brood-
ing originated in cheilostomes every time oogenesis was
altered within the broadcasting basal clades. If macrolecithal
oogenesis, and thus non-feeding larvae, evolved only once in
the evolutionary history of cheilostomes, then it is indeed
puzzling why a single extant species combining broadcast-
ing and lecithotrophy has not survived (see below for detailed
analysis).
3.4.1.1 Multiple Origins of Lecithotrophy
in Cheilostomata
Judging from the patchy distribution of planktotrophy in the
phylogenetic scheme of the bryozoan order Ctenostomata
(Todd 2000 ), brooding and lecithotrophy may have origi-
nated at least fi ve times in this group. I suggest the same
happened in the order Cheilostomata, which acquired brood-
ing (and thus lost planktotrophy) independently on several
occasions and at different geological times. Apart from
perhaps the superfamily Aeteoidea (see Jebram 1992 ),
brooding cheilostomes root their ancestry in the suborder
Malacostegina, which comprises only broadcasters and thus
lacks both lecithotrophy and parental care. In general, the
presence of lecithotrophic larvae in Bryozoa is always asso-
ciated with embryonic incubation, which, pari passu , never
goes hand in hand with a feeding larva. This means that, if
bryozoans with a planktotrophic larva and no parental care
were the ancestors of the clades with independently acquired
embryonic incubation, the endotrophic larva originated as
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
254
many times as incubation emerged. Thus, a shift in oogenesis
towards the origination of a non-feeding larval type was
always associated with (presumably preceded) the evolution
of parental care. If, instead, lecithotrophy has a monophy-
letic origin among Cheilostomata, then the above arguments
should be reconsidered, and one should expect the existence
of malacostegan-like cheilostomes without brooding but
with non-feeding larvae. Such variants are not yet known,
however, and the case of Arbocuspis bellula [formerly
Electra ], forming large eggs but considered to be a malaco-
stegan (Marcus
1938 ), requires further study.
Larval feeding is not known in either Phylactolaemata or
Stenolaemata, thus obscuring the question of whether a non-
feeding larva evolved independently in these classes or was
inherited from their ancestors. As for the class Gymnolaemata,
it seems that lecithotrophy evolved numerous times in both
its orders, Ctenostomata (Sect.
3.4.4 ) and Cheilostomata. If
the independent evolution of brooding is a marker for the
evolution of endotrophy, then in the cheilostome suborders
Inovicellina (having external membranous brood sacs) and
Scrupariina (having both external membranous sacs in skel-
etal bivalve ovicells) lecithotrophic larvae presumably
evolved independently in both clades. Judging from their
morphology, these suborders may have had different
malacostegan- like (i.e. non-brooding with planktotrophic
larvae) ancestors, although Inovicellina might also have
originated from a ctenostome ancestor [polyphyly of
Cheilostomata is demonstrated in the study by Jebram
(
1992 )]. Signifi cantly, the genera Scruparia (Scrupariina)
and Aetea (Inovicellina) group with malacostegans in a
molecular study by Waeschenbach et al. ( 2012 ). Also, the
non-feeding larva of Scruparia chelata is strongly reminis-
cent of the shelled cyphonautes-like larva of the ctenostome
Flustrellidra hispida but lacks the shell (see Barrois 1877 ;
Zimmer and Woollacott 1977a , b ).
Families Eucrateidae and Leiosalpingidae [both members
of suborder Scrupariina in Gordon ( 2012 )] brood their
embryos in external membranous sacs, similar to the situa-
tion in Aetea , while the supposedly related Scrupariidae have
bivalved ovicells. Since external sacs evolved several times
in both ctenostomes and cheilostomes, there is no obvious
connection between Aetea , Eucratea and leiosalpingids.
Similarly, the structure of the ovicell in the Scrupariidae dif-
fers from the conventional ovicells of other cheilostomes and
most probably evolved independently. Overall, it appears
that embryonic incubation evolved independently (twice?) in
Scrupariina.
Other examples include the cheilostome families
Calloporidae, Tendridae, Belluloporidae, Thalamoporellidae
and Alysidiidae: the structure of their cystids is easily derived
from that in malacostegans (directly or via intermediates),
and their brood chambers give evidence that these are non-
homologous. Thus, if these groups independently evolved
from the different malacostegan ancestors, the only group
known to have reproductive pattern I, then lecithotrophy
originated in them independently too. Incidentally, the
revealed topologies in two variants of the molecular analysis
made by Knight et al. ( 2011 ) indirectly confi rm the indepen-
dent origins of thalamoporellids (and their relatives, stegino-
porellids) and calloporids from malacostegans. Also,
according to Marcus ( 1939 ), the non-feeding larva of
Thalamoporella evelinae is only reminiscent of the larva of
Scruparia chelata – another cheilostome that seems to have
evolved brooding and lecithotrophy independently (see also
Zimmer and Woollacott 1977a ).
Important arguments supporting the hypothesis of multi-
ple and independent origins of lecithotrophy in cheilostome
bryozoans are (1) large time gaps between the apparent ori-
gins of groups with endotrophic larvae (as evidenced by the
fossil record), i.e. Calloporidae, Albian (Middle Cretaceous);
Scrupariidae, Maastrichtian (Late Cretaceous);
Thalamoporellidae, Eocene; Belluloporidae, Pleistocene;
Tendridae, Recent; and (2) the absence of direct phyloge-
netic connections between these taxa. I suggest that all of
these groups evolved from different malacostegine ancestors
(with cyphonautes larvae) and that lecithotrophy and brood-
ing originated in them independently. If the endotrophic
larva evolved only once, it follows that all of these groups
evolved from a hypothetical malcostegan-like clade with
lecithotrophy but without embryonic incubation. Moreover,
a further inference may be drawn that this clade had to sur-
vive from the Late Cretaceous until the present day. If this
scenario were correct, one would expect at least some such
cheilostomes (with a lecithotrophic larva but without brood-
ing) to have survived. A possible candidate is the previously
mentioned Arbocuspis bellula , an electrid malacostegan that
should be a broadcaster but is said to produce a large egg
(Marcus 1938 ) and may in fact be an internal brooder (see
Chap. 1 ). In their molecular analysis (which included data
from GenBank), Knight et al. ( 2011 ) found that this species
associated with species of Electra .
But even if lecithotrophy evolved once in the major chei-
lostome lineage Flustrina (=Neocheilostomina), currently
understood as monophyletic, anatomical data show that
brooding evolved numerous times within this lineage.
Accordingly, the new suborders Tendrina, Thalamoporellina
and Belluloporina, three new superfamilies, Tendroidea,
Thalamoporelloidea and Belluloporoidea, and the corre-
sponding family Belluloporidae are established herein (see
Appendix II for diagnoses). The case of Alysidiidae requires
additional study.
3.4.1.2 Tendra zostericola
Returning to the question of when embryonic incubation
evolved in respect to the origin of lecithotrophy, it should
additionally be noted that there are two opposing hypotheses
3 Evolution of Reproductive Patterns in Cheilostomata
255
concerning the origin of parental care and the evolutionary
enlargement of oocytes. Some authors think that the former
preceded the latter (Shine
1978 , 1989 ) and others, that the
reverse is true (Nussbaum
1985 , 1987 ; Summers et al. 2006 ).
Thus, theoretically the simplest variants of brooding might
have evolved in species with planktotrophic larvae. For
instance, some Streblospio polychaetes (Levin
1984 ; Levin
and Bridges 1995 ; Pernet and McArthur 2006 ) and the
kamptozoan Loxosomella elegans (Nielsen 1998 ) brood
small eggs that develop into planktotrophic larvae. Also,
some phoronid species brood their embryos within the ten-
tacle crown for several days, after which they leave the par-
ent organism to develop into planktotrophic actinotrocha
larvae (Silén 1954 ; Emig 1982 , 1983 ; Zimmer 1991 ). In this
phylum the smallest eggs are produced by non-brooding spe-
cies, however.
An interesting example in this respect is provided by the
reproductive pattern in Tendra zostericola , monotypic for
the genus (Tendridae) ( Electra pontica Gruncharova, 1980
is apparently synonymous). In the Black Sea this species
co- exists with Electra repiachowi , which produces
cyphonautes larvae. In contrast, T . zostericola (morphologi-
cally very close to Electra ) produces ciliated coronate lar-
vae whose early development occurs in the space between
the membranous frontal wall of the zooid and overarching
protective mural spines of the acanthostegal brood chamber
(Ostroumoff 1886a , b ; Braiko 1967 ; see also Sect. 2.3.5 ).
During reproduction, small oocytes (70 μm in diameter)
ovulate and accumulate in the coelom (4–10 in number; see
Nordmann 1839 ; Paltschikowa-Ostroumowa 1926 ; Braiko
1967 ; pers. obs.) of the maternal autozooid (Repiachoff
1875 ). After that they are transferred via the intertentacular
organ from the zooid cavity into the brood chamber. It is
unknown whether the ovary continues to form oocytes after
oviposition. Each zygote develops into a ciliated larva with
a non-functioning gut (Repiachoff 1875 , 1878 ; Ostroumoff
1886b ). According to Braiko ( 1967 ), the larvae of T . zosteri-
cola develop in the brood chamber in less than 10 h, whereas
Paltschikova- Ostroumowa ( 1926 ) wrote that they leave the
brood chamber after 2 days, meaning in both cases that lar-
val development is almost as fast as in the cyphonautes
embryo before it starts feeding. As with most bryozoan
endotrophic larvae, those of T . zostericola swim from 6–8
(warm water) to 24 h (cold water) before settlement (Braiko
1967 ). It should be also stressed that embryonic develop-
ment is successfully accomplished outside the brood cham-
ber in experiments (Braiko 1967 ).
These data provide evidence that the reproductive mode
of Tendra recapitulates an early stage in the evolution of
reproductive pattern II, showing a number of transitional
traits between broadcasters with planktotrophic larvae and
brooders with lecithotrophic larvae. On the one hand, Tendra
is morphologically very close to Electra , producing similar
number of small eggs of similar size. On the other hand,
these eggs possess enough yolk for larval development with-
out feeding. Tendra also has a primitive and independently
evolved brood chamber in which several embryos are
brooded simultaneously, developing to non-feeding larvae
with a rudimentary gut. Embryogenesis occurs in the water
entering the brood cavity in this species, which can be also
be adduced as a primitive trait since embryos of advanced
cheilostome brooders die when removed from ovicells to sea
water (see Silén 1945 ).
Structural and reproductive similarities between Tendra
and malacostegans may also demonstrate the possible mode
of transition to brooding in species with planktotrophic lar-
vae (similar to what occurs in phoronids and some poly-
chaetes, see above). For instance, instead of spawned zygotes
exiting into the water, the polypide might allow them to exit
onto the spine-fl anked frontal surface of the distal zooid,
which further transformed into an acanthostegal brood cham-
ber protecting the eggs from predators and/or silting. In con-
trast to extant brooders with endotrophic larva, ancient
brooders may have produced planktotrophic larvae in which
only the early stages of embryonic development took place
in such primitive brood chambers. The early stages of plank-
totrophic larval development have high development rates in
malacostegans. For instance, in Conopeum seurati , embryos
begin to move inside the fertilization envelope as early as 8 h
after spawning, leaving the envelope after 9 h. Early embryos
of Einhornia crustulenta (Electridae) complete this stage in
12 h. The gut becomes visible in the cyphonautes of the for-
mer species 32 h after the start of development (Cook 1962 ).
In Membranipora serrilamella the embryo begins to swim
slowly, while still enclosed within the fertilization envelope,
less than 24 h after spawning (using groups of cilia that pro-
trude through openings in the envelope). It starts to feed
2 days after spawning (Mawatari 1975 ). So, early cyphonautes
larvae could leave the brood chamber (had they originated
before endotrophy) very early, for instance, within the fi rst
2 days, as do the larvae of Tendra . In this case the transition
to a new mode of oogenesis and hence to an lecithotrophic
larva could occur in the future, after the evolution of brood-
ing, which would have increased survival of the still rather
numerous offspring.
Nevertheless, there are no living bryozoans with brood
chambers and planktotrophic larvae. If we consider that
brooding might have compensated for a reduction in the
number of offspring during the transition to lecithotrophy,
the lack of brooders with cyphonautes larvae may shed
light on the question of what came fi rst: lecithotrophy or
parental care? Species of Conopeum have fewer oocytes than
other malacostegans, and, possibly, relatively short-lived
cyphonautes larvae (Cook 1962 ; Dudley 1973 ). This perhaps
indicates an evolutionary trend towards a change in oogene-
sis mode accompanied by a reduction of the larval feeding
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
256
period in cheilostome broadcasters (Dudley 1973 ). If so,
brood chambers must have evolved some time after the
beginning of accumulation of additional nutrients in oocytes.
In this regard, we may recall that some sea urchins and sea
stars have lecithotrophic larvae that are not brooded but
develop in the external environment (Pearse and Cameron
1991 ; Byrne 1991a , b , 1995 , Byrne and Cerra 1996 ; Jeffery
and Emlet 2003 ; see for review Levin and Bridges 1995 ).
Incipient parental care in some of the orders of these classes
is considered to be the next evolutionary step (Byrne and
Cerra 1996 ), although phylogenetic analysis shows that in
some cases Echinoidea evolved brooding while bypassing an
endotrophic free-swimming larval stage (Jeffery and Emlet
2003 ). All of these arguments taken together would seem to
lend support to the hypothesis that brooding evolved in bryo-
zoans after the shift in oogenesis.
Whereas the vast majority of cheilostome brooders incu-
bate just one embryo, in a few species brood chambers con-
tain several embryos concurrently. Three to seven embryos
have been recorded in the ovicells of Scruparia chelata
(Hastings 1941 ; Mawatari 1973b ; Hayward and Ryland
1998 ), up to 10 in the acanthostegal brood chambers of
Tendra zostericola (see Braiko 1967 ), 2–3 in the ovicells of
Thalamoporella rozieri , four in T . californica and up to six at
various stages of development in T . evelinae (see Waters
1909 ; Hastings 1930 ; Marcus 1941a ; Chaney et al. 1989 ).
Three embryos of approximately the same size were seen in
the ovicells of Monoporella nodulifera ovicells (pers. obs).
Very large ovicells of Macropora levinseni (described by
Brown 1952 as M . grandis var. levinseni ) contain 2–4
embryos (Gordon 1970 ). I consider the presence of more
than one embryo in the brood chamber as a plesiomorphy,
characterizing early stages in the evolution of reproductive
pattern II, which originated on the basis of pattern I with
numerous oocytes. Notably, all of these bryozoans are repre-
sentative of early anascan-cheilostome clades with primitive
brood chambers, which presumably evolved independently
( Macropora and Monoporella have true ovicells). Two
embryos have occasionally been reported in ovicells of
Schizoporella unicornis (of different age, judging by their
colour; see Ross and McCain 1976 ) and Bugula foliolata (as
B . fl abellata ) (Corrêa 1948 ), and from two to several embryos
were recorded in the internal brood sacs of Oshurkovia lit-
toralis and Arctonula arctica (Eggleston 1972 ; pers. obs.). In
all of these cases, such multiple brooding may be considered
as an “atavism” from those times when the brood chamber
normally contained more than one embryo.
The above data are in accord with the suggestion that the
new (non-feeding) type of larva might have evolved rather
fast, while further increase in the size of oocytes was grad-
ual. By way of illustration, the descriptions and drawings of
Repiahoff ( 1875 , 1878 ) show the oocytes of Tendra zosteri-
cola as having relatively little yolk (apparently mesolecithal)
and the endotrophic larva has a rudimentary non- functioning
gut (see also Ostroumov 1886b ). Compared to all other
endotrophic cheilostome larvae that have been studied, the
Tendra larva forms fastest. So, sexual reproduction in Tendra
zostericola appears to correspond to the early stages in the
evolution of the new reproductive pattern in Gymnolaemata.
As in malacostegans, (1) the zooid still forms numerous
oocytes in cohorts, (2) oocytes ovulate in a group and exit
the visceral coelom of the maternal zooid one by one with
the help of the intertentacular organ, and (3) oocytes are
small and contain few nutrients, so embryogenesis is rapid.
As in brooders, there is incubation in a brood chamber, but
(1) the brooding time is short, (2) incubation occurs in
groups, and (3) the larva has a non-functioning gut. As dis-
cussed above, with this set of both plesiomorphic and apo-
morphic characters brooding could have evolved before as
well as after the transition to lecithotrophy.
Gradual evolution towards large macrolecithal oocytes
with plentiful nutritive reserves could have had two conse-
quences. Firstly, the duration of development up to the motile
larval stage was extended, as can be seen from a comparison
of the development time of T . zostericola larvae with the lar-
vae of other brooders (see Sect. 3.1.2 ). The physiological
mechanisms of this phenomenon remain obscure, but a simi-
lar tendency (slower development rate with increasing oocyte
size) is observed in some other invertebrates, for instance,
decapods (Clarke 1982 ). However, for bryozoan embryos
developing in brood chambers, such prolongation of devel-
opment was not risky.
Secondly, the number of simultaneously brooded embryos
gradually decreased to just one embryo. The antecedent mul-
tiple brooding mode was retained in only a few taxa. Some of
them, such as Thalamoporella , even have macrolecithal
oocytes (Marcus 1941a ). This combination of characters is
possible only if the brood cavity is very large, which is
indeed the case in Thalamoporella . The successively ripen-
ing macrolecithal oocytes appear to be transferred one by
one into the ovicell, which has room for several embryos.
Unfortunately, we have no information about oocyte type in
Scruparia , Macropora or Monoporella . Since Scruparia has
a lecithotrophic larva (and Macropora and Monoporella
almost certainly do as well), their oocytes should also have
an elevated nutrient content suffi cient for larval development
without feeding.
Three to seven oocytes are formed in the ovaries of the
malacostegan-like cheilostome “ Carbasea ” indivisa . After
ovulation they are transferred to the outside of the zooid and
brooded in clusters within external membranous sacs (Stach
1938 ), very similar to the situation in the ctenostome Triticella
fl ava (see above). In “ Carbasea ” indivisa and Tendra zosteri-
cola some of the embryos appear to develop faster than the
others (Paltschikowa-Ostroumowa 1926 ; Stach 1938 ), which
is probably due to a certain time gap in oviposition (the time
3 Evolution of Reproductive Patterns in Cheilostomata
257
when the eggs leave the maternal zooid). At the same time,
this gap is rather small – several older oocytes develop and
mature almost synchronously, as in Malacostegina. Also
Stach ( 1938 ) mentioned the irregular shape of ovulated
oocytes in “ C .” indivisa , which is also known in electrid
broadcasters. We do not know whether “ C .” indivisa and
T . zostericola have nurse cells like those in the majority of
studied cheilostome brooders; if they do not, this must also
indicate that their reproductive mode is an ancient one.
Examples of plesiomorphic simultaneous brooding of
several embryos in species with the most primitive brood
chambers (external membranous sacs and acanthostegal
brood chambers) are instructive. Most of the cheilostomes
with membranous sacs, as in the genera Aetea , Eucratea and
Leiosalpinx , brood a single embryo attached to the maternal
zooid (Fig.
2.52 ). Leiosalpinx australis sometimes has two
embryos (Gordon
1986 ). Cook ( 1977b ) reported that Aetea
anguina in one of the populations studied could have up to
two embryos in the same brood sac. External membranous
sacs may have evolved independently at least three times in
cheilostomes (see Chap.
2 ), and, as in ovicell brooders, the
above examples may point to the tendency towards a gradual
reduction in the number of oocytes (probably because of
their increase in size) in the species with brood sacs.
In conclusion, it should be emphasized that the data pre-
sented in this section indicate that both lecithotrophic larvae
and parental care evolved many times in different cheilo-
stome lineages. Brooding evolved independently at least 7–8
times. In all of these cases the ancestors appear to have been
broadcasting malacostegans with planktotrophic larvae. The
acquisition of embryonic incubation was each time accom-
panied (preceded or followed) by the evolution of a non-
feeding larva.
3.4.2 Fertilization and Modifi cation
of Oogenesis
In the hypothesized scenario concerning the evolution of
brooding from an antecedent broadcasting mode of sexual
reproduction, the transition to macrolecithal oogenesis was
accompanied by a shift to early fertilization, which might
have been a precondition for the origin of nurse cells. These,
in turn, could have additionally enhanced the effectiveness of
vitellogenesis (see Sect. 3.2 ).
Theoretically, the increase in the amount of nutrients con-
tained in oocytes may have had another reason behind it. As
discussed in the review by Wourms ( 1987 ), there may be a
connection between the time of fertilization and the charac-
ter of oocyte formation. In some invertebrates the fusion of
the male and the female gametes results in dramatic changes
in oogenesis. Some rotifers (for instance, Euchlanis dilatata
and Brachionus rubens ) exhibit enormous differences in the
quantity and quality of yolk in their oocytes depending on
whether or not the female has been inseminated (Gilbert
1983 , 1989 ), and fertilization may well be the reason for
these differences (Gilbert
1989 ). In other words, in these
rotifers the fertilized oocyte somehow infl uences the func-
tioning of the vitellarium (the part of the ovary synthesizing
yolk and transporting them to the oocyte). In another
Brachionus species, B . calycifl orus , sperm are known to fuse
with early oocytes. In other words, the presence of the sperm
may determine the growth character of the female gamete, in
particular, the mode of vitellogenesis.
Although intraovarian fertilization is a generally rare phe-
nomenon, it is obviously obligatory in all Bryozoa incubating
their offspring (in broadcasters the male and female gametes
fuse during ovulation). Thus, its role, especially its infl uence
on oogenesis in Bryozoa, may be considerable. Having in
mind the example of the rotifers, one may suggest that the
entry of sperms into the ovary and subsequent fertilization
there could additionally stimulate vitellogenesis. In brooding
cheilostomes, early fertilization ultimately resulted in the
complete dependence of oogenesis on sperm arrival. Fusion
of sperm with early oocytes became the trigger for vitellogen-
esis (see also Sects.
1.3.4 and 1.3.6 ). This evolutionary nov-
elty is of paramount importance – the colony does not have to
spend energy and nutrients on vitellogenesis before receiving
the sperm, that is, before fertilization is guaranteed (Bishop
et al. 2000 ). As long as vitellogenesis has not started, the col-
ony may invest more resources into somatic growth, for
example, and a larger colony can fi lter a greater volume of
water, increasing the chances of obtaining alien sperm.
How this trait (dependence of vitellogenesis on syngamy)
was retained during evolution is an intriguing question.
How could an external factor (entering of alien sperm) infl u-
ence the genetic programme in such a way as to prevent vitel-
logenesis before syngamy? Crucial prerequisite was an ability
of the young oocyte to fuse with sperm very early (before the
onset of vitellogenesis). Further, early syngamy became an
obligatory stage for oocyte development, and indispensable
for the start of vitellogenesis. In this connection, information
concerning the time of fertilization in Tendra zostericola is
crucial. One may speculate that in this species with many
primitive characters fertilization occurs during ovulation (as it
does in malacostegans) and nurse cells are absent. If this is
true, the onset of vitellogenesis in Tendra , contrary to all other
brooding cheilostomes, does not depend on fertilization.
Intraovarian fertilization is unlikely to infl uence vitello-
genesis in Ctenostomata, however, as indicated by the fact
that in the ctenostome Bowerbankia gracilis late macroleci-
thal oocytes are fertilized (Temkin 1996 ).
Another important consideration is that internal fertiliza-
tion would seem to be a necessary prerequisite for the incu-
bation of embryos during the evolution of invertebrates
(Ryland and Bishop
1993 ). In the view of Temkin ( 1994 ),
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
258
evolution towards intracoelomic incubation is problematic
because of the need for the larva to escape from the zooid.
Fertilized oocytes should exit the zooidal cavity before the
onset of brooding, otherwise the exit of a large, “solid” larva
would need to be accompanied by rupture of the cystid wall.
Intracoelomic fertilization should dramatically increase the
chances of oocytes to be fertilized but would require a physi-
ological mechanism preventing cleavage before oviposition.
Such a mechanism must have evolved in phylactolaemates
and most gymnolaemates.
Cyclostomes and epistomiid cheilostomes, on the other
hand, were not handicapped by such apparent inherent diffi -
culties and succeeded in evolving intracoelomic incubation.
In the former, the isolation of the gonozooid coelomic cavity
during larval release appears to be ensured by the structure of
the vestibulum and the membranous sac (see Borg
1926 ).
Also, larvae are fl exible enough to squeeze through the nar-
row tube of the ooeciostome. In epistomiids, maternal zooids
do not develop polypides and cease to function after larval
release (Dyrynda and King 1982 ).
3.4.3 Oviposition in Cheilostome Brooders
Bryozoan polypides exhibit a broad range of “individual” and
collective behaviours associated with feeding, cleaning the
lophophore and the colony, avoidance of unfavourable exter-
nal factors and gamete release (Cook 1977a , 1980 ; Winston
1977 , 1978 ; Shunatova and Ostrovsky 2001 , 2002 ; Ostrovsky
and Shunatova 2002 ; Ostrovsky et al. 2002 , 2008a ). To place
a fertilized oocyte into the ovicell, the polypide has to per-
form a complex behavioural act, transferring it from the coe-
lomic cavity of the maternal zooid into the cavity of the brood
chamber via the supranerval pore or, in some species, the
intertentacular organ (see also Sects. 1.3.7 and 1.3.9 ).
Compared to the spawning of eggs via the intertentacular
organ in broadcasting species (Silén 1966 ; Temkin 1994 ), the
act of oviposition is much more complex. Apparently, it
evolved in cheilostomes at about the same time as brooding.
The origin of brooding must have resulted in the loss of
the intertentacular organ. Perhaps the removal of large eggs
from the coelom of maternal zooids was fraught with more
diffi culties than oviposition via the supraneural pore. This
limitation does not seem to apply to Tendra zostericola , in
which the mature oocytes are relatively small, and to
Thalamoporella evelinae , whose female zooids have a very
large intertentacular organ and brood cavity. In the event, an
analogue of the intertentacular organ evolved in two
Schizoporella species (see Sect. 1.3.9 , also discussed in
Ostrovsky and Porter
2011 ).
The evolutionary scenario may be sketched as follows.
In the fi rst brooding cheilostomes with primitive endotrophic
larvae the zygotes were attached to the distal zooid, surrounded
by a sticky fertilization envelope as in some ctenostomes
(see Ström
1969 ). Upon leaving the maternal zooid, zygotes
remained between the mural spines on the proximal gymno-
cyst of the distal zooid. The chances of becoming attached to
this particular area of the distal zooid were high, since the
coelomopore is placed between distomedial tentacles and the
introvert of the expanded polypide is often inclined in this
direction. Oviposition can also be accompanied by polypide
tilting. It is also rather probable that such species still had an
intertentacular organ, involved in oviposition. Such special-
ized behaviour is characteristic of some ctenostomes (see
Sect. 3.4.4 ).
Following the evolution of skeletal brood chambers from
the mural spines, the fertilized oocyte had to be placed into
the brood cavity. It was presumably at that evolutionary
moment that the fi rst ovicelled cheilostome lost the interten-
tacular organ.
Judging from the descriptions of oviposition in the litera-
ture, large eggs are removed from the visceral coelom in
brooding bryozoans by means of (1) increased pressure of
the coelomic fl uid of the maternal zooid and (2) high plastic-
ity (fl exibility) of the oocytes (see Sect. 1.3.7 ). Coelomic
fl uid pressure is increased by contraction of parietal muscles,
which lower the frontal membrane or expand the ascus. The
polypide is automatically protruded in the process but the
supraneural pore is situated much higher than the entrance of
the brood chamber. To transfer an egg into the brood cavity,
therefore, the lophophore should be protruding only par-
tially, so that the base of the tentacle crown and its coelomo-
pore are just opposite the ovicell entrance. The ovulated
oocyte should by that time be near the supraneural pore.
Presumably, when this latter condition is in place, the pres-
sure of the coelomic fl uid is increased by appropriate con-
traction of parietal muscles, resulting not in full protrusion of
the polypide but in the extrusion of the large oocyte from the
maternal body cavity. The polypide remains in this position
for several minutes, until the zygote is transferred into the
brood chamber. Oviposition under a closed operculum
appears to be secondary development, evolving after the ori-
gin of cleithral ovicells (see Sect. 1.3.7 ).
It follows that this process of oviposition must have
evolved within the order Cheilostomata as many times as
skeletal brood chambers did.
3.4.4 Evolution of Sexual Reproduction
Within the Order Ctenostomata
3.4.4.1 Reproductive Patterns and Evolutionary
Trends
Analysis of the relevant literature shows that the general evo-
lutionary direction of the reproductive patterns in cteno-
stomes was the same as in cheilostomes. Most ctenostomes
3 Evolution of Reproductive Patterns in Cheilostomata
259
brood their embryos, with only four species in four different
families having cyphonautes larvae – Alcyonidium albidum
(Alcyonidiidae), Farrella repens (Triticellidae),
Hypophorella expansa (Hypophorellidae) and Hislopia
malayensis (Hislopiidae) (Ström
1977 ; Zimmer and
Woollacott
1977a ; Wood 2008 ; Nielsen and Worsaae 2010 ).
The reproductive mode and early development of both F .
repens , described by Marcus (
1926a ), and H . expansa (see
Prouho 1892 ) indicate that their larvae are truly cyphonautes,
but their later stages, although presumably shelled, are
unknown (discussed in Zimmer and Woollacott 1977a ;
Waeschenbach et al. 2012 ). Nevertheless, the presence of the
intertentacular organ in many Alcyonidium species and some
other ctenostomes (see Table 1.9 , reviewed in Ostrovsky and
Porter 2011 ) indicates that planktotrophy is not so rare in this
order. Some ctenostomes also have matrotrophic brooding
(reviewed in Ostrovsky et al.
2008a ; see also Ostrovsky and
Schwaha
2011 ).
The diversity of reproductive patterns in ctenostomes is
an inviting fi eld of study, promising a detailed reconstruction
of the evolutionary stages of sexual reproduction not only
within this order but within the whole phylum. At present,
most descriptions of ctenostome sexual reproduction in the
literature contain only a perfunctory characterization of
oogenesis and often one cannot be sure about the exact
reproductive pattern. Besides, the productivity of the female
gonad throughout the reproductive period has never been
assessed, and the numbers of oocytes in the ovary and the
coelom as well as the numbers of brooded embryos (see
below and Table 3.2 ) refl ect only the state of things at the
moment of study/collection. Therefore, the account that fol-
lows may be somewhat incomplete and imprecise, and
should be treated as a fi rst attempt at revealing the evolution
of sexual reproduction in ctenostomes based on the data in
the literature.
Reproductive pattern I in Ctenostomata is similar to that
in Cheilostomata. Numerous (from 10–15 to 60) small
oocytes 25–90 μm in diameter are formed in the ovary. Most
or some of them ripen, ovulate (in groups of 5–15 oocytes),
are fertilized and released. These eggs are oligolecithal and
develop into planktotrophic larvae. Apparently this pattern
was also characteristic of the earliest ctenostomes.
Other reproductive patterns in ctenostomes differ in some
respects from the corresponding patterns of cheilostomes.
Pattern II is characterized by the brooding and production
of lecithotrophic larvae that develop from oocytes containing
more nutrients than oocytes in species with pattern I.
Ctenostomes appear to have several variants of pattern II,
differing in the number and size of female gametes formed in
the ovary and in the number of brooded embryos (see
Table 3.2 ), viz (1) several dozen small oocytes are formed in
the ovary, attaining 65 μm diameter upon maturation; then
they ovulate (up to 60), are released and externally brooded
in groups of 2–4 up to 20, each developing into non-feeding
larva ( Triticella fl ava ); (2) 20–40 small female gametes are
formed in the ovary but apparently only 4–8 of them mature,
being rather large (>100 μm diameter); then they ovulate, are
released and brooded externally, usually one by one
( Paludicella articulata , Potsiella erecta ); (3) from 4 to 10–12
or even 19 oocytes are formed in the ovary; upon maturation
they can be small (50–90 μm), medium-sized (100–200 μm)
or large (>300 μm); further, the eggs ovulate, are released
and brooded in groups of 2–6 (up to 12) ( Alcyonidium
duplex , A . polyoum , A . eightsi , A . hirsutum , A . diaphanum ,
Tanganella muelleri , T . appendiculata , Bulbella abscondita ,
Panolicella nutans ); (4) 1–5 relatively small (80–90 μm) or
very large (up to 370 μm) oocytes are produced in the ovary,
ovulate sequentially, and are brooded in the introvert one by
one ( Bowerbankia imbricata , B . gracilis , B . pustulosa ,
Alcyonidium disciforme , Terebripora comma ). Judging from
the illustrations in the literature, different species of brood-
ing non-matrotrophic ctenostomes have mesolecithal or
macrolecithal oocytes with a size range from small to very
large. The above pattern II variants may be arranged in a
series representing a trend towards a gradual decrease in
number and increase in size of the produced oocytes and the
brooded embryos.
Pattern III is characterized by small eggs, extraembryonic
nutrition and endotrophic larvae. Contrary to cheilostome
matrotrophs with pattern III that produce a small number of
oocytes (usually 1–2 doublets) and brood embryos one by
one, such ctenostomes produce from 2–3 to 100 female gam-
etes, of which 1–10 mature as small oligo- or mesolecithal
oocytes; they ovulate and are brooded one by one or in
groups of 2–5, considerably enlarging during embryogene-
sis. Ctenostome species that appear to have pattern III, judg-
ing from the available descriptions and illustrations, are
Labiostomella gisleni , Sundanella sibogae , Nolela dilatata ,
N . stipata , N . gigantea , Walkeria uva , Bantariella cookae
and Zoobotryon verticillatum .
The ctenostome Flustrellidra hispida supposedly has
reproductive pattern IV. The ovary produces 4–5 gametes
that grow into relatively small macrolecithal oocytes about
100 μm diameter and after ovulation are brooded simultane-
ously in a brood chamber (Pace 1906 ). Larval enlargement
indicates the presence of extraembryonic nutrition.
Nevertheless, despite the advanced brooding type,
Flustrellidra hispida has a primitive endotrophic pseudocy-
phonautes larva with chitinous valves and a rudimentary gut.
If we take pattern I as the starting point, the evolution of
sexual reproduction in the order Ctenostomata may be repre-
sented as follows:
(1) The transition from pattern I to pattern II was con-
nected with the origin of ctenostomes with primitive brood-
ing in external sacs and numerous small oocytes in the
ovary, which, however, accumulated enough nutrients for the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
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 indi-
cated 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 ten-
dency 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 reproduc-
tion 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 ves-
tibulum 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 ves-
tibular 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 invagina-
tion 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 pre-
requisite of the origin of placental analogues and extraem-
bryonic 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 diam-
eter, 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 indi-
cate 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 hap-
pened in Cheilostomata. Although incubating only one to a
few embryos, these species still produce numerous, rela-
tively 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 cteno-
stome 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 some-
times modifi ed: 4–11 embryos are brooded simultaneously
in Alcyonidium hirsutum ; 6–12 in A . eightsi ; 4–6 in A . poly-
oum ; 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 sin-
gle 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, modi-
fi 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
261
1960 ; Hayward 1985 ). Because the polypide degenerates,
the mature oocyte is not released in the environment and gets
from the maternal coelom into the pouch via the ciliated fun-
nel that is formed.
Judging from the distribution of the reproductive pat-
terns across the Ctenostomata, brooding in the introvert has
also independently evolved in several other ctenostome
superfamilies: Vesicularioidea (described in Bowerbankia
gracilis , B . pustulosa , B . imbricata , Amathia lendigera , A .
semiconvoluta , Vesicularia spinosa , Buskia nitens ),
Walkerioidea ( Walkeria ), Terebriporoidea ( Terebripora sp.,
Spathipora comma , S . mazatlanica ) and Victorelloidea
( Immergentia suecica ) (Joliet
1877 ; Braem 1951 ; Reed
1988 ; Calvet 1900 ; Bobin and Prenant 1954 ; Prenant and
Bobin 1956 ; Soule and Soule 1969a , 1975 , 1976 ; Ström
1977 ; Hayward 1985 ). All these species brood one embryo
at a time.
The brooding of embryos in introverts, as with brood-
ing in invaginations of the body wall, is a precursor to
matrotrophy. Increase in embryo size is known in Walkeria
uva and Bantariella cookae (Walkerioidea) and in
Zoobotryon verticillatum (Vesicularioidea) (Joliet 1877 ;
Waters 1900 ; Zirpolo 1933 ; Banta 1968 ; Ström 1977 ;
Ostrovsky et al. 2008a ; Ostrovsky and Schwaha 2011 ).
Judging from the considerable enlargement of their
embryos during brooding, these species have reproductive
pattern III. Embryo enlargement has also been noted in
Flustrellidra hispida (Alcyonidioidea), in which 4–8
embryos develop in the introvert (Prouho 1889 ; Pace
1906 ; Hayward 1985 ) but this species has macrolecithal
(though not large) oocytes and thus conforms to reproduc-
tive pattern IV.
(4) Boring ctenostomes of the genus Penetrantia
(Penetrantiina) evolved yet another incubational variant,
brooding embryos one at a time in an unusual outer embryo
sac of which the structure and development are poorly known
(Silén 1947 ; Soule 1950b ; Soule and Soule 1969a , b , 1975 ;
Ström
1977 ). Also, data on oogenesis in this group are virtu-
ally non-existent.
Thus, the trends in the evolution of sexual reproduction in
Ctenostomata associated with brooding were as follows:
• an increase in oocyte size – from small oocytes (30–
90 μm) in broadcasters towards larger ones (65–370 μm)
in brooders (and, as a consequence, a transition from
planktotrophic to lecithotrophic larvae);
• an overall decrease in the number of gametes formed in
the ovary as well as a decrease in the number of maturing
oocytes;
• a transition from a group mode to an “individual” mode of
oocyte maturation, ovulation and release/oviposition;
• a transition from external to “mixed” brooding and to
internal brooding in the introvert, or from external brood-
ing to brooding in an invagination of the body wall;
• the origin of extraembryonic nutrition.
Apart from the trends associated with the evolution of
brooding, this list closely resembles those in the order
Cheilostomata (see Sects. 3.1 and 3.3 ).
The diversity of brooding modes in the order Ctenostomata
illustrates two trends in the evolution of parental care (Braem
1951 ; Ström 1977 ; Jebram 1985 ; Smith et al. 2003 ).
Ctenostomes lack both a rigid skeleton and structures that
could serve as a basis for the formation of protective brood
chambers. This may be the reason why their brooding evolved
towards “intrazooidal” incubation, that is, (1) transfer of
embryos into body-wall invaginations or (2) the introvert cav-
ity. Interestingly, no viviparous ctenostomes have been found.
The simplest and least-reliable brooding mode is that of
attaching adhesive fertilization envelopes of the released
oocytes to the cystid or the introvert of the maternal zooid.
This primitive variant was the basis for the evolution of two
more-advanced ones, when oocytes attached to the cystid
wall are submerged into its invaginations or are transferred
into the vestibulum cavity during retraction of the polypide.
The origin of such specialized behaviour as the polypide
attaching eggs specifi cally to the protruding introvert in
Bulbella abscondita , Tanganella muelleri and Alcyonidium
duplex (see Prouho 1892 ; Braem 1951 ) was a prerequisite of
“internal” brooding, since the retraction of the polypide
entailed transfer of the attached eggs into the vestibulum
cavity. In T . muelleri , embryos are in addition submerged
into the vestibulum wall, after which the polypide degener-
ates. “Mixed” brooding, exemplifi ed by B . abscondita and A .
duplex , characterizes an intermediate stage in the evolution
of “internal” brooding (see Braem 1951 ); the polypide con-
tinues to function and the embryos remain in the vestibulum
only when the polypide is retracted. Additionally it should
be stressed here that these two species possess an interten-
tacular organ, the larva of B . abscondita has a rudimentary
gut and the gutless larva of A . duplex has a triangular
cyphonautes shape (Prouho 1892 ; Braem 1951 ; Zimmer and
Woollacott
1977a ), all clearly pointing to an independent
transition to lecitotrophy accompanied by the evolution of
embryonic brooding.
Thus, fertilized ovulated eggs were initially transferred
into the introvert cavity by the polypide. In the more advanced
variant, oocytes were transferred into the brood cavity with-
out leaving the cystid. Polypide degeneration and obligatory
brooding (either in the vestibulum cavity or in a specialized
chamber substituting for the introvert) resulted in physical
isolation of the embryo from a range of impacts. Some
ctenostomes brood several embryos at a time whereas in oth-
ers a single large embryo develops in the introvert. These
differences appear to be explained by differences in oogene-
sis and in the capacity of the introvert – the more nutrients
are accumulated in oocytes, the fewer eggs may be formed
and brooded in a zooid. In Alcyonidium gelatinosum the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
262
brood cavity is enlarged by means of a voluminous brood
pouch developed in place of the degenerated tentacle sheath.
In addition, this species has a ciliated funnel facilitating the
transfer of oocytes to the place of brooding.
Imperfect as it may have been, attachment of zygotes to
the surface of the spinose distal zooid in primitive brooding
cheilostomes undoubtedly provided a degree of protection
and may thus be considered as a form of parental care.
Perhaps the presence of spines may have prevented cheilo-
stomes from evolving brooding within the introvert. On the
other hand, should we consider the attachment of oocytes to
a spineless zooidal surface, as occurs in some cheilostome
and ctenostome species, a form of brooding? Such attach-
ment provides no mechanical protection but may ensure, for
instance, that the zygotes do not fall onto an inhospitable
substratum prior to becoming motile (Note that, in contrast
to the embryos of endotrophic larvae, those of planktotro-
phic larvae become motile very soon). In Bulbella abscondita ,
zygotes detached from the zooid reportedly cease to develop
(Braem
1951 ), but the reasons for this are unknown and the
data need verifying. In the ctenostome Triticella fl ava and
the cheilostome Tendra zostericola , eggs develop normally
even after removal from the brood chamber (Ström 1969 ;
Braiko 1967 ), but such zygotes would have little chance of
surviving in nature and any form of brooding is likely to
result in a considerably higher survival rate.
It is suggested here that the adhesive properties of the fer-
tilization envelope that sticks to the zooidal wall after egg
release could be a result of changes in the chemical composi-
tion of oocytes during transition to a new mode of oogenesis.
Such adhesive envelopes are known in different groups of ver-
tebrates and invertebrates (Adiyodi and Adiyodi 1989 , 1990 ;
Lombardi 1998 ). In malacostracan crustaceans, for instance,
such eggs are brooded and develop into late larvae (Adiyodi
and Subramoniam 1983 ), testifying to the high nutrient con-
tent in oocytes. In bryozoans, oocytes with an increased
amount of yolk (the basis for transition to endotrophy) could
adhere to the maternal colony to develop on its surface. As
noted above, bryozoans with this type of brooding, as well as
all the other brooding species, have non- feeding larvae. The
subsequent emergence of brood chambers in cheilostomes,
and brooding in the modifi ed introvert or body-wall invagina-
tions in ctenostomes, facilitated better protection of embryos.
Thus, modifi cation of oogenesis would be conducive to reten-
tion of embryos in the colony as a precondition for the origin
of brooding – supporting the hypothesis that modifi cation of
oogenesis preceded the origin of brooding.
3.4.4.2 Parallel Evolution of Sexual Reproduction
in Different Superfamilies of
Ctenostomata
The general trends that have emerged so far – the shift from
broadcasting to brooding and the increase in oocyte size
accompanied by decrease in oocyte number – give insight
into the evolution of sexual reproduction in the different
superfamilies of Ctenostomata.
The known ctenostome superfamilies apparently differ-
entiated as early as the lower Paleozoic – in the Early
Ordovician according to Todd (
2000 ). The distribution of
larval types and modes of parental care within these super-
families, as well as their positions in the phylogenetic tree,
show that ctenostomes evolved lecithotrophic larvae and
brooding several times [at least fi ve times judging from the
data in Ström (
1977 ), Zimmer and Woollacott ( 1977a ) and
Todd ( 2000 )]. The superfamilies Alcyonidioidea (one of the
basal groups), Victorelloidea and Walkerioidea (terminal
groups) comprise both brooders and species with
cyphonautes larvae, with brooders constituting the majority.
According to Todd ( 2000 ), Walkerioidea and Victorelloidea
are sister groups of the superfamily Vesicularioidea, which
comprises brooders only. If so, then the common ancestor of
these three families had a planktotrophic larva that was lost
independently (in connection with the evolution of brood-
ing) in each of the clades. Unfortunately, almost nothing is
known about reproduction in the superfamilies Hislopioidea
and Arachnidioidea apart from the facts that the freshwater
genus Hislopia has a cyphonautes larva (Wood 2008 ) and
Cryptoarachnidium argilla has an intertentacular organ, i.e.
is supposedly a broadcaster (Banta 1967 ); thus both super-
families comprise species with a planktotrophic larva and
reproductive pattern I. In the superfamily Paludicelloidea,
only primitive external brooding has been described (Braem
1896 ). Thus, parental care has been recorded in representa-
tives of fi ve out of seven ctenostome superfamilies, as well
as in Labiostomella , which according to Todd ( 2000 ) groups
with Protoctenostomata. Three of them include species with
embryonic incubation as well as broadcasting, pointing to at
least three instances of independent evolution of parental
care and non-feeding larvae among ctenostomes. However,
since such groups have both basal (Alcyonioidea) and ter-
minal (Walkerioidea, Victorelloidea) positions on the cteno-
stome phylogenetic tree, it seems that this happened six
times in this order.
Within the Alcyonidioidea, independently evolved leci-
thotrophy and brooding characterizes the family Alcyonidiidae
and the genus Alcyonidium . The latter is a very rare example
of a bryozoan genus with both planktotrophic and lecithotro-
phic larvae and patterns I and II. Moreover, in Alcyonidium
duplex , a brooder with a lecithotrophic larva, oviposition
occurs via the intertentacular organ, as in non- brooding bryo-
zoans, and its larva has a triangular cyphonautes shape (Farre
1837 ; Prouho 1892 ). Alcyonidium species also demonstrate
two brooding variants (brooding in the introvert and “mixed”
brooding) and different modes of oogenesis, corresponding to
the above-discussed trends towards the formation of fewer,
larger oocytes. Flustrellidra hispida (Flustrellidridae), which
3 Evolution of Reproductive Patterns in Cheilostomata
263
may belong to the same superfamily, has evolved matrotro-
phic incubation (reproductive pattern IV).
Broadcasting in Victorella pavida and V . pseudoarach-
nidia (see Braem 1951 ; Jebram and Everitt 1982 ) (although
the actual larvae are unknown), lecithotrophy and various
modes of parental care including extraembryonic nutrition
(that is, reproductive patterns I, II and III) have been
recorded in the superfamily Victorelloidea. The evolution of
brooding in this group proceeded from attachment of
oocytes to the cystid ( Pottsiella erecta ) to their immersion in
the cystid wall ( Tanganella appendiculata , Panolicella
nutans ) and, on this basis, the origin of matrotrophy ( Nolella ,
Sundanella ) as well as temporary ( Bulbella abscondita ) or
“permanent” ( Immergentia suecica , Spathipora comma , T .
muelleri ) retraction of embryos into the introvert. In the lat-
ter species the embryos are also immersed in the vestibulum
wall. Also, the lecithotrophic larva of B . abscondita has a
rudimentary gut.
Cyphonautes larvae ( Farrella repens , Hypopharella
expansa ) and coronate larvae, external ( Triticella fl ava ) and
internal (in the introvert) brooding as well as extraembryonic
nutrition ( Walkeria uva , Bantariella cookae ) have been
described in the superfamily Walkerioidea. This means that
this ctenostome group, too, is characterized by reproductive
patterns I, II and III.
In all species of the superfamily Vesicularioidea, embryos
develop in the introvert, but the phylogenetic position of this
group indicates that their ancestry featured a planktotrophic
larva. The only mode of brooding in this superfamily is in the
introvert, and Zoobotryon verticillatum has extraembryonic
nutrition. Hence, this superfamily possesses reproductive
patterns II and III.
A comparison of the reproductive variants among the
ctenostome clades shows that the evolution of brooding in
each of them followed a similar or the same scenario – from
external to internal brooding in an invagination of the body
wall and/or introvert. The occurrence of planktotrophy and
lecithotrophy within the same groups indicates multiple inde-
pendent origins of non-feeding larvae within Alcyonidioidea,
Walkerioidea, Victorelloidea and Vesicularioidea. As in the
Cheilostomata, lecithotrophy always accompanies brooding,
which may point to a connection between these two phenom-
ena. It is quite possible that the endotrophic larva evolved in
ctenostomes as often, and approximately at the same time, as
brooding did. The simplest mode of external brooding is
found in the freshwater ctenostome Paludicella articulata
(superfamily Paludicelloidea). Judging from the position of
Paludicelloidea in the phylogenetic tree of ctenostomes,
brooding evolved independently in this group also.
The above comparative analysis of reproductive patterns
in ctenostome bryozoans illustrates one possible trend in the
evolution of oogenesis in this order – a reduction in the num-
ber of oocytes produced or maturing in a zooid. Although the
total number of female gametes forming in the ovary of most
ctenostomes is still rather considerable, relatively few of
them mature and are brooded. An apparent trend towards
oocyte enlargement is also indicated but it is not so well
expressed as in cheilostomes. Additionally, as in cheilo-
stomes, brooding may compensate for the decrease in the
number of maturing eggs in ctenostomes. In general, these
evolutionary pathways are accompanied by a shift to leci-
thotrophy strongly reminiscent of the scenarios suggested
for Cheilostomata.
Another important aspect of ctenostome evolution is the
independent origin of matrotrophy in different clades (super-
families). Embryonic enlargement is recorded within the
Alcyonidioidea, Walkerioidea, Victorelloidea and
Vesicularioidea, as well as in Labiostomella gisleni . The
immersion of eggs in the zooid wall or their transfer to the
introvert for incubation, thereby isolating the brood cavity
from the external medium and also allowing physiological
exchange between the oocyte and the cystid wall, may have
promoted the evolution of the embryophore in some cteno-
stomes. The available data indicate that extraembryonic
nutrition evolved in ctenostomes at least fi ve times.
3.4.4.3 Parallel Evolution of Reproductive
Patterns in Ctenostomata and
Cheilostomata
Summing up the above comparisons, the reproductive pat-
terns in the Ctenostomata are similar or identical to those in
the Cheilostomata (the only exception being viviparity,
which is unknown among ctenostomes). The evolution of
sexual reproduction in these two orders as well as in different
ctenostome superfamilies shows similar trends, with many
novelties originating more than once, independently and at
different times. Distinct parallels observed in ctenostomes
and cheilostomes may be connected to the phylogenetic
relatedness of these two groups, the Ctenostomata being
paraphyletic with respect to Cheilostomata. Actually, the
same general trends are characteristic of all Bryozoa, and a
change in one character (the acquisition of a novelty) trig-
gered a similar cascade of morphogenetic events, although
these transformations sometimes involved different struc-
tures. Increasing oocyte size (accompanied by a decrease in
their number) was the basis for the evolution of lecithotro-
phy. The origin of a non-feeding larva in bryozoans must
have been somehow associated with the origin of embryonic
incubation, with different structures being involved in the
formation of brood chambers (spines, kenozooids, body-wall
invaginations and evaginations). Further, parental care
changed from external brooding towards the more reliable
internal mode. In its turn, internal incubation (brooding or
viviparity) was a prerequisite for the origin of extraembry-
onic nutrition, with matrotrophic structures being evolved
on the basis of ovaries (Cyclostomata, Cheilostomata), a
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
264
membranous sac (Cyclostomata) and the body wall
(Ctenostomata, Cheilostomata, Phylactolaemata).
The examples of Triticella fl ava (Ctenostomata), Tendra
zostericola and “ Carbasea ” indivisa (Cheilostomata), which
have small oocytes and brood several embryos simultane-
ously, show that the lecithotrophic larva does not require a
considerable increase in the amount of nutrients in oocytes
(as in echinoderms; see Byrne et al.
2003 ), and that the evo-
lution of lecithotrophy is not a very diffi cult evolutionary
step (Christiansen and Fenchel 1979 ; see also below). Since
nutrient resources in the egg are limited, such a larva should
be fast-developing and short-lived. At the same time, the
number of oocytes formed in the ovary remains considerable
despite an increase in the amount of nutrients in the egg. This
combination of characters, together with the presence of
endotrophic larvae with a rudimentary gut, should be consid-
ered as transitional from plesiomorphic pattern I towards
more-derived patterns. As with pattern IV, which combines
attributes of patterns II and III, this transitional pattern com-
bines features of patterns I and II.
Both ctenostomes and cheilostomes with reproductive
pattern II show similar “overlaps” of various kinds. The pres-
ence of numerous female gametes in the ovary, only some of
which mature and are later brooded in some way, was
described in some ctenostomes but also occurs in cheilo-
stomes (Cribrilinidae, Margarettidae). Some cheilostomes
( Scruparia , Thalamoporella , Macropora , Monoporella )
have multiple brooding, characteristic of ctenostomes from
various families, whereas the development of embryos of
different ages in the ovicells of Thalamoporella is reminis-
cent of, for example, the ctenostome Nolella . In those cheilo-
stomes that are primitive external brooders ( Aetea , Eucratea ,
Leiosalpinx ), 1–2 embryos are normally incubated at a time
(see Cook 1977b ; Eggleston 1963 ; Gordon 1986 ) and this is
combined with a rather small number of maturing oocytes
(Waters 1896 [1898] ). Reproduction in some ctenostome
species is reminiscent of this variant.
In comparing species with pattern III, the main difference
between the two bryozoan orders is in the number of oocytes
in the ovary. There are many in some ctenostomes and only a
few in cheilostomes. In consideration of the differences in
oogenesis, I suggest that pattern III evolved in these two
gymnolaemate clades on a different basis. In Cheilostomata,
placental analogues apparently fi rst evolved in species with a
few macrolecithal oocytes (pattern IV), and oocytes became
oligolecithal later (pattern III) (see Sect. 3.3 ). A similar tran-
sition from pattern II to pattern IV could have also occurred
in some ctenostomes, for instance in Flustrellidra hispida ,
which combines macrolecithal oocytes with extraembryonic
nutrition. Besides, placental analogues evolved indepen-
dently in some ctenostomes with both large ( Labiostomella
gisleni , Nolela dilatata ), and relatively small ( Walkeria
uva , Zoobotryon verticillatum ) numbers of small oocytes.
I denote this variant as pattern III, based on the fact that it
combines matrotrophy, relatively small oocytes (micro- or
mesolecithal judging from published illustrations) and
noticeable embryonic enlargement. In the former case (com-
bination of matrotrophy with many eggs in ovary), embry-
onic brooding evolved fi rst, but there was no reduction in egg
number (although only few of them were incubated). Further,
matrotrophy evolved but the quantity of eggs produced
remained high. In the latter case (combination of matrotrophy
with few eggs), the transition to brooding was accompanied
by a reduction in the number of oocytes. In the evolution of
this pattern, as in Walkeria uva and Zoobotryon verticilla-
tum , transitions from patterns II to III and IV to III were both
theoretically possible in ancestors. In this connection we should
once again recall the Phylactolaemata, in which pattern III
evolved independently from Ctenostomata and in which
there are also a relatively large number of small eggs in the
ovary and sequential incubation of individual embryos.
Theoretically, an evolutionary scenario involving matrot-
rophy in combination with the production of numerous small
oocytes is not to be excluded for brooding cheilostomes, since
several species among them do produce numerous (although
macrolecithal) oocytes. If the oocytes of their ancestors con-
tained fewer nutrient reserves (a transitional pattern charac-
teristic of Tendra zostericola and “ Carbasea ” indivisa ), then
the possibility existed for matrotrophic (possibly multiple)
brooding to evolve in combination with mesolecithal oogen-
esis. Further changes in oogenesis (transition to fewer macro-
lecithal oocytes) or extraembryonic nutrition (enhanced
activity of the embryophore accompanied by a reduction in
the number of oocytes) could have resulted in patterns IV and
III, respectively. To emphasize, the above scenario is purely
speculative, since no placental cheilostomes are known to
have numerous oocytes in the ovary.
3.4.5 Environmental Factors and Radiation
of Cheilostomata in the Late Cretaceous
The upper half of the Cretaceous witnessed an explosive
radiation of Cheilostomata (Lidgard et al. 1993 ; Gordon and
Voigt 1996 ; Jablonski et al. 1997 ; Taylor 2000 ), apparently
triggered by the acquisition of a lecithotrophic larva (Taylor
1988a ; see also Taylor and Larwood 1990 ). This novelty
seems to appear several more times in cheilostome history,
being a result of changes in oogenesis and the production of
larger, more nutrient-rich eggs. The ecological factors that
infl uence, directly or indirectly, organismal development
(Schmalhausen 1949 , 1982 ; Jablonski and Lutz 1983 ;
Matsuda
1987 ; Balon 1991 ; McEdward 1995 ; Wray 1995b ),
including larval types (discussed in Wourms
1987 ), suppos-
edly drove egg enlargement. Wray ( 1995a ) listed a number
of factors that might infl uence egg size in invertebrates with
3 Evolution of Reproductive Patterns in Cheilostomata
265
planktotrophic larvae, including selection for increased post-
metamorphic survivorship (by producing large juveniles)
and selection for reduced larval mortality caused by preda-
tion and seasonal food fl uctuations (by shortening the free-
swimming period) (see also Jablonski and Lutz
1983 ;
Nielsen
1995 , 1998 ; Clarke 1992 ; Jeffery 1997 ).
From this perspective, non-feeding larvae are more expe-
dient if planktonic food availability is low and non-stable,
and vice versa. For instance, species of congeneric sea
urchins inhabiting opposite coasts of the Isthmus of Panama
have different egg sizes and larval types, refl ecting differ-
ences in productivity in the Pacifi c and Atlantic coasts of the
isthmus – planktotrophic larvae are found in the highly pro-
ductive Pacifi c waters while lecithotrophic ones are charac-
teristic of the Atlantic with a relative paucity of planktonic
food (Lessios
1990 ; Jaeckle 1995 ). Lessios ( 1990 ) suggested
that these differences in egg size are not a result of differ-
ences in the environment of the adults, but an adaptive
response to the primary productivity of the oceans in which
larval development occurs. At the same time, planktotrophy
can be retained if species switch to seasonal reproduction,
with periodic decreases in the amount of available food com-
pensated for by correspondingly timed breaks in reproduc-
tion (see Todd and Doyle 1981 ).
With reference to Thorson’s rule, Jeffery ( 1997 ) sug-
gested that multiple independent origins of lecithotrophy and
brooding in sea urchins in the Late Campanian–Maastrichtian
were associated with the gradual cooling of the ocean and
abrupt fl uctuations in phytoplankton abundance. These con-
ditions, according to Jeffery, promoted the loss of plankto-
trophic larvae in at least nine sea urchin clades. Temperature
fl uctuations in the ocean in the very end of the Cretaceous
have been effectively proven (Barrera and Savin 1999 ), sup-
porting Jeffery’s hypothesis. According to Emlet ( 1990 ),
echinoids lost planktotrophic larvae at least 14 times. To
note, brooders among living sea urchins are confi ned to the
cold, seasonal waters of the Antarctic and Subantarctic
(Emlet et al.
1987 ; Emlet 1990 ; McNamara 1994 ), with
brooding having originated independently in the Echinoidea
in these regions at least three times (Poulin and Féral
1996 ).
As for marine bryozoans, they may “reduce” planktotro-
phy in the process of colonizing non-stable estuarine habitats
(Dudley 1973 ). This hypothesis was based on a comparison
of the sizes and life spans of cyphonautes larvae in different
broadcasting cheilostomes (malacostegans) and on observa-
tions of their colonial development. So, based on Dudley’s
information about the whole life cycle of these epibionts, it
is reasonable to suggest that the transition from a long to a
short free-swimming larval period could be explained by the
shift to an “opportunistic” life strategy in unstable habitat
that involves a “shortening/accelerating” of both larval and
colonial development.
An opposing point of view concerning developmental
evolution would be that it is not larvae, but adults that are
“responsible” for the origin of a non-feeding mode. Chia’s
(
1974 ) hypothesis suggests that a transition to lecithotrophy
may be triggered by an acute shortage of resources. If less
food is available to adults, it is expedient to have fewer lar-
vae/juveniles that are larger and develop faster. In other
words, if resources are scarce, populations decrease in num-
ber but this decrease is offset by a higher survival rate of
larvae/juveniles. Valentine (cited by Strathmann
1986 ) simi-
larly suggested that the energy available to adults infl uences
the evolution of larval development (see also Clark and
Goetzfried 1978 ). Availability of food to parents during the
reproductive period was also considered in Todd and Doyle’s
( 1981 ) model.
Food is generally accepted to be the most important envi-
ronmental factor infl uencing reproduction (see Strathmann
1986 ; Kasyanov 1989 ; Eckelbarger 1994 ). In many marine
invertebrates the quality of maternal nutrition is refl ected in
oocyte parameters such as size and content (see reviews by
Jaeckle 1995 ; Havenhand 1995 ). In particular, observations
and experiments on echinoids show that there is a correlation
between adult feeding and egg quality. In Strongylocentrotus
droebachiensis , eggs produced by individuals having plenti-
ful or scanty food contained different amount of lipids
(Thompson 1983 ). Sea urchins Arbacia lixula taken from
habitats with different levels of food produced eggs of differ-
ent size with different amounts of proteins and lipids; if there
was more food, the eggs were larger and contained more
yolk (George 1990 ; George et al. 1990 ; reviewed in Jaeckle
1995 ). Dependence on exogenous factors be seen in the data
of Krug ( 2007 ), who has shown that in winter and spring up
to half the individuals in the populations of the poecilogonic
snail Alderia willowi lay numerous small eggs from which
long-lived planktotrophic larvae develop, whereas in sum-
mer most snails lay a few large eggs from which lecithotro-
phic larvae develop. An increase in the number of snails
laying small eggs generally correlates with the cooling and
freshening of water. Thus, it seems that in summer abundant
food for adults facilitates production of large eggs and non-
feeding larvae with rapid development irrespective of the
abundance of plankton, whereas winter food depletion stim-
ulates production of numerous eggs and planktotrophic lar-
vae that will develop to juveniles and settle temporally nearer
to a summer period. A similar observation concerning the
correlation between food stability for adults and larval type
was made by Clark and Goetzfreid ( 1978 ).
Large-scale environmental changes are among the cru-
cial factors that might induce changes in developmental
modes (Matsuda
1987 ; Levin and Bridges 1995 ; Jablonski
2005 ). Taking the Albian (that is, the beginning of the Late
Cretaceous diversifi cation of Cheilostomata) as the starting
point, we are faced with the onset of global biosphere
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
266
changes caused by active underwater volcanism (Leckie
et al.
2002 ). An important feature of the Late Cretaceous
was a powerful increase in oceanic productivity, particularly
expressed as a pulse of the dominant skeletal phytoplank-
tonic groups, which constitute the lion’s share of the bryo-
zoan diet (Winston
1977 ). It is in the Cretaceous that the
peak of microplankton diversity was achieved (Rigby and
Milsom
2003 ). Owing to global warming, accompanied in
the Late Cretaceous and especially in the Albian–Turonian
by a considerable sea-level rise (Poulsen et al. 1999 ; Leckie
et al. 2002 ; Skelton 2003 ), several groups of planktonic
algae also reached the peak of their diversity and abundance.
Having originated in the Early Jurassic, Coccolithophyceae
had their fi rst heyday in the beginning of the Late Jurassic,
then again in the Aptian and Albian, reached the peak of
their abundance in the Maastrichtian (Late Cretaceous)
(Haq
1983 ; Bown 1998 ; Skelton 2003 ). The diversity of sili-
cofl agellates (Dictyochophyceae) (Haq
1983 ; Martin 2003 )
and diatoms (Bacillariophyceae) (Racki 1999 ; Martin 2003 )
also somewhat increased in the late Cretaceous. However,
these algal groups, though found in the gut of bryozoans
(Hunt 1925 ; Winston 1977 ; pers. obs.), are nevertheless of
secondary importance in their diet because of their hard cal-
careous or siliceous skeletons. It is therefore all the note-
worthy that the diversity of dinofl agellates (Dinofl agellata)
skyrocketed in the Albian (Martin 2003 ), when brooding
cheilostomes evolved. These unicellular organisms consti-
tute a signifi cant, if not the major component of a bryozoan
diet. Dinofl agellate diversity fell abruptly in the Turonian
but was soon (in the Santonian) followed by another peak,
almost as high as that in the Albian (Williams and Bujak
1985 ; Fensome et al. 1996 , 1999 ). It should be noted that the
Late Cretaceous was also the time of increased diversity of
planktonic Radiolaria (diversity peaks falling on the Aptian/
Albian boundary, Late Albian and Maastrichtian) and
Foraminifera (Silva and Sliter 1999 ; Leckie et al. 2002 ;
Skelton 2003 ).
The heydays of planktonic algae must have been favour-
able for invertebrates with planktotrophic larvae (McEdward
and Miner 2003 ). However, such periods should be favour-
able not only for such larvae but also for adult fi lter-feeding
animals. Increased plankton abundance impacts the epiben-
thos, being expressed in increased productivity of benthic
assemblages. Not surprisingly, one of the diversity peaks of
Bivalvia, in particular rudists, is in the Albian–Cenomanian
(Cox et al. 1969 ). As for bryozoans, which are a crucial com-
ponent of many bottom communities, food has been experi-
mentally shown to have the strongest impact on the various
aspects of their life activity. Changes caused by surplus or
shortage of food, listed in the reviews by Winston (
1977 ) and
Jebram (
1978 ), include growth rate and the shape and size of
colonies as well as zooids. Plentiful food naturally causes an
increase in these parameters. Additionally, experiments show
that the abundance and composition of the diet directly infl u-
ence when bryozoan colonies reach sexual maturity.
To sum up, it is possible that increased abundance of food
might itself be a favourable backdrop to facilitating shifts in
oogenesis, transitioning to lecithotrophy in some cases. The
secular correlation between the rapid diversifi cation of chei-
lostomes and increasing phytoplankton diversity and abun-
dance is notable, but there are other ecological factors that
could also add to bryozoan success in the Late Cretaceous.
The Cenomanian witnessed global marine transgressions
(Hancock and Kauffman 1979 ; Johnson 1999 ), which,
according to Larwood ( 1979 ) and Voigt ( 1981 ), could have
affected the evolutionary fate of Cheilostomata. A similar
idea was voiced by Ross and Ross ( 1996 ) for Paleozoic bryo-
zoans – global sea-level rise coincided with an increase in
bryozoan diversity, while its fall coincided with periods of
extinction (discussed in Taylor and Ernst
2004 ). As for
Cheilostomata, as compared to the preceding Albian, in the
Cenomanian vast areas of shallow sea provided epibionts
with a broad range of econiches, which, in combination with
a high abundance of phytoplankton and ongoing movements
of the continents (Skelton
2003 ) should have promoted spe-
ciation. This coincidence between global environmental
changes and the onset of the cheilostome radiation was also
noted by McKinney et al. ( 2001 ). Bryozoan diversifi cation at
this time could also have been enhanced by an increase in
predation (Vermeij 1977 ). Bryozoans are obligatory or facul-
tative food targets for many different animals (McKinney
et al. 2003 ; Lidgard 2008a , b ) and predation was likely a
factor of paramount importance for their evolution (Lidgard
et al. 2012 ). Many structures acquired by cheilostomes in the
Late Cretaceous (spines, avicularia, strongly calcifi ed frontal
shields and frontal budding, ovicells) are considered to have
been protective adaptations that evolved in response to the
emergence or increase in predation (Larwood and Taylor
1981 ; McKinney et al. 2003 ). As for frontal (opesial) spines,
their presence may be considered a preadaptation in the ori-
gin of brood chambers. In addition, the transition to a short-
lived endotrophic larva would also have been advantageous
against increasing predation pressure (see Nielsen 1998 ).
It should be emphasized that progressive colonial integra-
tion was a key to the success of Cheilostomata. They evolved
polymorphism (including sexual polymorphism) and brood-
ing morphofunctional modules consisting of autozooids with
ovicells and avicularia (Lidgard et al. 2012 ). The broad dis-
tribution of these structures within the order indicates their
effectiveness in enhancing the survival of colonies.
Relevant to the discussion about causality in the transition
to lecithotrophy are the results obtained by MacLeod and
Huber (
1996 ). According to these researchers, the Late
Cretaceous was characterized by global changes in oceanic
circulation, that is, reorganization of the vertical transfer of
water masses. Theoretically, such large-scale events would
3 Evolution of Reproductive Patterns in Cheilostomata
267
have impacted the biota. Vertical transfer of water masses
caused by changes in their temperature and salinity inevita-
bly entail changes in horizontal transfer. At the same time,
the reproductive success of a population is determined,
among other things, by favourable hydrological conditions
(Kasyanov 1989 ). Planktotrophic larvae, which are com-
pletely dependent on currents (Shanks
1995 ), could have
been eliminated in the open ocean, being unable to settle in
suitable sites (Mileikovsky 1971 ). Bryozoans with short-
lived larvae would have had an evolutionary advantage in
this situation.
A number of gymnolaemate bryozoans retained plankto-
trophic larvae. The broad distribution of such species,
ensured by long-lived larvae, seems to be an effective means
of withstanding local extinctions (Jablonski and Lutz 1983 ),
highlighting the dispersal value of such larvae (Strathmann
1978b ). There is, however, another viewpoint, according to
which the possibility of long-distance dispersal is a by-
product of the transition to a safer and better-supplied life in
the plankton (Strathmann
1985 , 1990 ).
Finally, in the Early and the Late Eocene, coccolithophores
achieved another diversity peak, comparable to that in the
Late Cretaceous (Haq 1983 ; Bown 1998 ). At the same time,
dinofl agellates (Williams and Bujak 1985 ; Fensome et al.
1996 , 1999 ) and, to some extent, silicofl agellates (Haq 1983 )
also fl ourished. Ascophoran cheilostomes experienced
explosive diversifi cation at the same time (Voigt 1985 ). Also,
it is in the Eocene that one third of the genera evolved whose
Recent representatives have placental analogues (see above).
3.4.6 Possible Consequences of Transition
to the New Reproductive Pattern
According to Taylor’s ( 1988a ) hypothesis, the evolution of
lecithotrophy in Cheilostomata considerably shortened the
duration of the dispersal stage and triggered very high rates
of speciation for most of the Late Cretaceous (about 40 mil-
lion years) (see also Taylor and Larwood 1990 ). These rates
as well as the number of taxa (both brooding and broadcast-
ing) peaked at the Campanian–Maastrichtian boundary and
then fell abruptly with the catastrophic extinction event at the
Cretaceous–Paleocene (К–Т) boundary. Diversifi cation rates
recovered rather fast, however, and cheilostomes continued
to diversify from the Early Eocene to Late Miocene (another
40 million years). For the last ten million years diversifi ca-
tion rates of cheilostomes have been decreasing, demonstrat-
ing, nevertheless, a continuously positive dynamic (Taylor
2000 ; McKinney et al. 2001 ).
At the same time, in analyzing the evolutionary success of
Cheilostomata, we have to take into account a number of
external and internal factors that could have supported it.
While generally agreeing with Taylor’s (
1988a ) hypothesis,
Gordon and Voigt ( 1996 ) nevertheless asked: could lecithot-
rophy, once acquired, have sustained high speciation rates
for so long? The above authors put forward their own hypoth-
esis, according to which the progressive radiation of cheilo-
stome bryozoans was based on the evolution of new types of
protective skeletal frontal shields. The evolution of leci-
thotrophic larvae and brooding can be considered as a trigger
of radiation, later sustained by the evolution of skeletal struc-
tures. Boardman and Cheetham (
1973 ) and Cheetham and
Cook ( 1983 ) considered as a key factor in the success of
Cheilostomata a combination of increased colonial integra-
tion, plasticity of different characters and evolution of com-
plex frontal shields with the increasing range of habitats in
the Late Cretaceous and the Cenozoic as a background. The
evolution of vertical forms of colonial growth also contrib-
uted considerably to success (McKinney 1986a , b ; McKinney
and Jackson
1989 ). Among other possible factors, the evolu-
tion of zooidal polymorphism and modular complexity
should not be forgotten (Silén
1977 ; Cheetham and Cook
1983 ; McKinney and Jackson 1989 ; Lidgard et al. 2012 ).
Polymorphism in cheilostomes is expressed not only by vari-
ous forms of zooids but also extrazooidal units, frequently
spines, that themselves can be adapted for various function-
alities. In fact, each ascophoran zooid is a construction con-
sisting of the autozooid and its frontal shield (ancestrally
derived from fl attened kenozooidal overgrowths) or/and
extrazooidal modules (Gordon and Voigt 1996 ; Lidgard et al.
2012 ). Cormidial association with adventitious avicularia
and ovicells (also evolved from spines) make such construc-
tions even more complex. The various permutations and
combinations of cormidial elements have been a major factor
in the diversifi cation and evolutionary success of cheilo-
stomes, but further analysis is contingent upon “evo-devo”
studies in bryozoans. And last but not least, cheilostomes
evolved brooding. The origin of spines and protection of the
frontal wall and embryos enhanced survival of bryozoans in
the face of predation pressure. At the same time, the primi-
tive spinocyst and ooecium became the basis for evolution-
ary more advanced and reliable protective structures.
Increased phytoplankton abundance in combination with
sea-level rise, geographic isolation and other biotic and abi-
otic factors would have provided very favourable conditions
for increasing speciation rates of cheilostomes in the Late
Cretaceous. The heyday of bryozoans in the Eocene also
coincides with high phytoplankton abundance, but another
important factor may have been the vacation of many niches
after the К–T extinction (for general discussion see, for
instance, Maynard Smith 1989 ; Erwin 2001 and references
therein).
One of the crucial factors that might have contributed to
the diversifi cation of cheilostomes was the fact that species
with lecithotrophic larvae could colonize free econiches at
greater depths. Cyphonautes larvae are mostly confi ned to
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
268
the upper sea layers with phytoplankton, whereas non-
feeding larvae may disperse and settle much deeper. Most
Recent broadcasting bryozoans do not exist below 100–
200 m, two exceptions being Pyripora catenularia and
Electra arctica , which can be found as deep as 500–520 m
(Kluge 1975 ; Prenant and Bobin 1966 ; Hayward and Ryland
1998 ; also discussed in Taylor 1988a ). Conversely, bryozoan
brooders have even colonized the abyss down to 8300 m
( Bugula sp.; see Hayward 1981 ). The evolution of endotro-
phic larvae apparently revoked food restrictions, providing
bryozoans with a pass to deepwater biotopes. To note, the
early malacostegans that existed in the Late Jurassic proba-
bly inhabited shallow coastal zones (Taylor 1994 ).
Diversifi cation rates could to some extent be supported by
multiple origins of lecithotrophy. The transition to endotro-
phic larvae probably occurred in cheilostomes as many times
as brooding evolved (see above), each time potentially trig-
gering speciation, although these events obviously have not
contributed signifi cantly to overall cheilostome diversity
(see Taylor 1988a ).
Yet another weighty factor ensuring successful
competition at the very beginning of the epibiotic phase of
the bryozoan life cycle is the enlargement of the ancestrula
– a result of larval metamorphosis. Greater energy input into
a single offspring should enhance its survival (Smith and
Fretwell 1974 ). In other words, larger offspring size should
considerably reduce mortality. One important conclusion
made during many studies is that most of the nutrient
resources accumulated in the egg are not used during embry-
onic and larval development, being reserved for peri- and
postmetamorphic periods (Emlet and Hoegh-Guldberg 1997 ;
Byrne and Cerra 2000 ; Byrne et al. 2003 ; Marshall and
Bolton 2007 ). In other words, parents provision their larvae
with more reserves than they need, thus increasing post-
metamorphic performance (reviewed in Emlet et al. 1987 ).
Experiments on the removal of some lipids (50% of organic
mass) from the blastulae of the sea urchin Heliocidaris
erythrogramma have shown that embryos develop into ana-
tomically correct but small (non-feeding) larvae as fast as
lecithotrophic larvae in the controls (Emlet and Hoegh-
Guldberg 1997 ). The authors concluded that much of the
nutrient contained in oocytes is not used during embryogen-
esis and is later “placed at the disposal” of the juvenile. So,
the tendency towards increasing oocyte size is likely to be
associated with increasing viability of the young sea urchin;
enlargement of oocytes could increase survival rate of young
after larval settlement and metamorphosis.
Larval size infl uences pre- and post-metamorphic perfor-
mance in cheilostome bryozoans. In Bugula species the
larger larvae swim and remain capable of metamorphosis
longer than smaller larvae (Wendt 2000 ; see also Wendt
1998 ). Field observations on Watersipora subtorquata
showed that larger larvae swim longer and are more selective
with respect to settlement substrata (Marshall and Keough
2003 ; see also Elkin and Marshall 2007 ). In this species the
larger a competent larva, the larger the juvenile (ancestrula),
and larger ancetrulae have better chances of survival (dis-
cussed in Marshall and Keough 2004a ). Further, larger
ancestrulae bud larger zooids and so develop into larger colo-
nies. As shown in W . subtorquata , growth rate, size and sur-
vival rate of colonies are directly correlated with increasing
larval size (Marshall and Keough 2004a , 2008a ). Experiments
with Bugula neritina revealed a positive correlation between
larval size and downstream survival, growth rate, onset of
reproduction, fecundity and fi nal colony size (Marshall et al.
2003 ; Marshall and Keough 2004b , 2006 ; reviewed in
Marshall and Keough 2008b ; Marshall et al. 2008 ).
Hence, the evolution of larger eggs, and, consequently,
larvae could result in the success of the adults. McKinney
(
1992 , 1993 , 1995 ) showed that Recent Cheilostomata,
because of larger size and some morphological features, are
more effective energy consumers than Cyclostomata, also
expressed in faster growth rates of colonies (also discussed
in McKinney et al.
2001 ). As a result, beginning in the Late
Cretaceous, larger and faster-growing cheilostomes began to
dominate over cyclostomes in marine bottom communities
(Taylor and Larwood 1988 ). This dominance was expressed
as more-frequent fouling of cyclostome colonies by cheilo-
stomes and more-numerous cheilostome colonies as com-
pared to cyclostomes, in the same biotopes and in greater
number of cheilostome taxa. Thus, Cheilostomata was over-
all more competitive because cheilostome colonies were
larger. McKinney ( 1993 ) and Pachut and Fisherkeller ( 2010 )
also showed that cheilostome larvae are larger than those of
cyclostomes.
Chia ( 1974 ) noted that juveniles of marine invertebrates
developed from planktotrophic larvae are usually smaller
than those that develop from lecithotrophic ones. However,
in regard to Cheilostomata, we should not forget that exotro-
phic larvae enlarge considerably as they feed and grow. For
instance, in Membranipora serrilamella the diameter of ovu-
lated oocytes is 50 μm, the width of the cyphonautes larvae
base by the time it becomes triangular is 220 μm and that of
the adult larvae is over 600 μm. The size of twinned ances-
trulae in this species is 630–680 × 470–550 μm (Mawatari
and Itô 1972 ; Mawatari 1973a , 1975 ; Mawatari and Mawatari
1975 ) (see also Table 3.1 ).
To note, the size of ancestrulae may vary depending on
abundance of food. According to Cook ( 1964 ), Electra
monostachys ancestrulae formed in September were smaller
(180 × 100 μm) than those formed in July (240 × 200 μm).
It may be suggested that the evolution of Malacostega
went towards larger larvae and correspondingly larger ances-
trulae. The size of ancestrulae of the earliest known cheilo-
stome Pyriporopsis portlandensis (Tithonian, Late Jurassic)
was 240–230 × 200–170 μm. Two other malacostegans from
3 Evolution of Reproductive Patterns in Cheilostomata
269
the Late Cretaceous had ancestrulae of the following size –
Spinicharixa pitti (?Aptian): 160 × 140 μm; Herpetopora
laxata (Campanian–Late Maastrichtian): 220–200 × 120–
110 μm (Taylor 1986a , b , 1988b ). Recent malacostegans
have much larger ancestrulae (Table
3.1 ) and, correspond-
ingly, larvae, indicating a distinct evolutionary trend.
The trend towards increasing ancestrular size probably
also characterized brooding bryozoans. The size of the
ancestrulae in eight species of the earliest-known (Albian)
cheilostome genus Wilbertopora with brooding varies in the
range 260–230 × 190–150 μm (Cheetham et al. 2006 ). So,
there is no signifi cant difference in the size of ancestrulae
(and, apparently, larvae and oocytes) in the fi rst Malacostegina
(broadcasters) and the fi rst Calloporidae (brooders). This
means that the transition to a new pattern of oogenesis, a new
larval type and the origination of brooding did not result in
any signifi cant increase in ancestrular size. In the course of
further evolution oocyte size gradually increased, a trend that
in many marine invertebrates is accompanied by brooding
(Wray 1995a ).
Enlargement of oocytes inevitably affected the sizes of
larvae and ancestrulae. Since the transition to lecithotrophic
larvae seems to have required only a relatively small increase
in the amount of nutrients in oocytes (see the examples of
Tendra zostericola and Triticella fl ava ), the accumulation of
extra reserves and consequent enlargement of ancestrulae
could have been an important factor infl uencing the success
of Cheilostomata. We may also speculate that accumulation
of additional reserves in oocytes would accelerate the forma-
tion of the ancestrula and the budding of daughter zooids,
also improving the survival chances of the young colony.
Based on data in the literature, Pachut and Fisherkeller
( 2010 ) calculated the average diameter of the ancestrula in
Recent brooding cheilostomes to be 220 μm. This is slightly
more than the average size of ancestrulae in Wilbertopora
(207.5 μm) (see Cheetham et al. 2006 ). However, in order to
fi nd out whether a trend can be identifi ed using ancestrular
size, much more data are required for both Recent and fossil
bryozoans.
3.5 Evolution of Sexual Reproduction
in Bryozoa
Lecithotrophy, embryonic incubation and internal fertiliza-
tion are characteristic of all three classes of phylum Bryozoa.
Loss of planktotrophy and the acquisition of parental care
occurred repeatedly within each of the two gymnolaemate
orders Ctenostomata and Cheilostomata. The fact that all
bryozoans with planktotrophic larvae have internal fertiliza-
tion indicates that bryozoans acquired this fertilization mode
early in their evolutionary history or it was inherited from an
ancestor. Later transition to early intra-ovarian fertilization
occurred independently in Phylactolaemata, Cyclostomata
and Cheilostomata. Moreover, if different groups of brood-
ing cheilostomes evolved independently from different mal-
acostegan ancestors, this transition might have occurred
several times within this order alone. Early intraovarian fer-
tilization presumably did not happened in Ctenostomata
since sperm has so far been found only in growing and late
oocytes.
As for the loss of planktotrophy and the evolution of
parental care, Phylactolaemata either inherited a non-feeding
short-lived larva from their marine ancestor or evolved it
independently. The recent fi nding of a cyphonautes larva in a
freshwater ctenostome of the genus Hislopia (Wood 2008 ;
Nielsen and Worsaae 2010 ) demonstrates that planktotrophic
bryozoan larvae can exist in fresh water. The reproductive
pattern of phylactolaemates combines primitive and
advanced characters – numerous small oocytes (20–40
according to Wood ( 1983 ) and up to 42 in Lophopus crystal-
linus , 25 μm in diameter; see Marcus 1934 ), placental brood-
ing (which phylactolaemates evolved independently),
intraovarian fertilization and putative nurse cells (in
Lophopus ). A very similar combination of characters is
found in the “protoctenostome” Labiostomella gisleni (Silén
1944 ). In both Phylactolaemata and L . gisleni numerous
small oocytes are formed in a maternal zooid but only one of
them develops into a larva in the brood sac with extraembry-
onic nutrition. The larva L . gisleni is unknown but we may be
fairly sure that it is endotrophic.
In Phylactolaemata brooding could have originated either
in the early phylactolaemates or in their marine ancestor.
Oocyte transfer into the brood sac, bypassing the environ-
ment, which is characteristic of Phylactolaemata (see Brien
1953 ), has not been found in any marine bryozoan. The
brood sacs of phylactolaemates are formed on the oral side
of the zooid, while in gymnolaemates they are formed on the
anal side (Jebram 1973 ). Thus, these structures, although
both being invaginations of the body wall, are not homolo-
gous. This means that Phylactolaemata evolved brooding
independently. Invagination of the cystid wall, which is trig-
gered by the adhesion of the released oocyte in Ctenostomata,
could be triggered by the ovary, which always closely adjoins
the brood sac in Phylactolaemata. At the same time, this
invagination could have originally appeared in connection
with external brooding, which later was substituted by the
internal mode.
In summary, the reproductive features of Phylactolaemata
generally correspond to pattern III as described for the
ctenostomes L . gisleni and Nolella dilatata . Although a
fertile phylactolaemate zooid broods one embryo at a time,
the number of oocytes in the ovary remains large. This pat-
tern might have evolved on the basis of pattern II (as
described for ctenostomes, see Sect. 3.4.4 ) in connection
with the acquisition of the placental analogue. Importantly,
3.5 Evolution of Sexual Reproduction in Bryozoa
270
phylactolaemates possibly have nurse cells (Marcus 1934 ;
see also Sect.
3.2 ).
I would like to note that the data presented in this book
call for a reconsideration of the defi nitions of reproductive
patterns II, III and IV. In Gymnolaemata, pattern II should
include all cases of non-matrotrophic brooding, and patterns
III and IV all cases of placental brooding combined with,
correspondingly, oligo-/meso- and macrolecithal oogenesis.
At the same time, the number of oocytes may vary
considerably.
As for the class Stenolaemata, the reproductive pattern of
Recent Cyclostomata (viviparity) is similar to pattern V in
the cheilostome family Epistomiidae. Undoubtedly, this is an
example of convergence. Having found that ancestrula size is
similar in Recent and fossil stenolaemates, Pachut and
Fisherkeller ( 2010 ) suggested that polyembryony is a mono-
phyletic trait in this class. This leads to the conclusion that
incubation and the endotrophic larva in general have evolved
in the class only once.
Branching structures in Cystoporata, stenolaemates from
the Late Ordovician, are considered as chambers for embry-
onic incubation (Buttler 1991 ; see also Taylor and Larwood
1990 ). If so, non-feeding larvae evolved at least by the Late
Ordovician in stenolaemates. Chambers for embryonic incu-
bation (termed ovicells) have often been reported in
Fenestrata (Stratton 1975 , 1981 ; Southwood 1985 ; Bancroft
1986 ; Morozova 2001 ). However, judging from their struc-
ture and the suggested relationships between these two
Paleozoic stenolaemate orders (McKinney 2000 ), they are
unlikely to be homologous with the putative incubation
chambers of cystoporates. In Cyclostomata, zooids for
embryonic incubation (gonozooids) originated as late as the
Late Triassic (Taylor and Michalik 1991 ). Thus, incubation
structures seem to be not homologous within this class.
On the other hand, incubation itself would have originated
only once. Early stenolaemates, including Paleozoic cyclo-
stomes, could have retained non-feeding larvae in the peri-
stome, the distal part of the cylindrical autotozooid (Borg
1926 ; Taylor and Larwood 1990 ). If so, and if endotrophy
evolved only once in Stenolaemata (or was inherited from an
ancestor), embryonic incubation in the specialized chambers
originated independently at different times in different
stenolaemate orders on the basis of incubation in non-
modifi ed zooids. Of course, this conclusion would also hold
true if the endotrophic larva evolved several times in stenolae-
mates, as was apparently the case in gymnolaemates.
It is not known if Paleozoic cyclostomes incubated their
progeny, allowing the possibility that they might have
evolved an endotrophic larva much later, when gonozooids
evolved. Before that their larvae may have been planktotro-
phic, as indicted by the low taxonomic diversity of this group
in the Paleozoic (Ernst and Schäfer 2006 ). In contrast, other
Paleozoic stenolaemate orders were rather species-rich and
hence possibly had a non-feeding larva. Finally, cyclostomes
may be polyphyletic; they may have evolved from two differ-
ent ctenostome ancestors (Ernst and Schäfer 2006 ), and
those that evolved in the Mesozoic would then have newly
acquired gonozooids, endotrophy and polyembryony.
Whatever the case, Cyclostomata evolved viviparity, that
is, intracoelomic incubation of embryos accompanied by
extraembryonic nutrition. The sequence of evolutionary
events may have been similar to the case of Ctenostomata
(see above), involving external brooding by means of adhe-
sion of embryos to the lophophore, retraction of embryos
into the introvert (“mixed” brooding), obligatory brooding in
the tentacle sheath accompanied by polypide degeneration
and, fi nally, embryonic development in the coelomic cavity
of the zooids and then in the ovary. A similar scenario (except
for brooding in the tentacle sheath) appears possible in the
Epistomiidae, whose ancestors probably brooded their
embryos in ovicells.
The presence of only one or two oocytes in the ovary may
indicate that viviparity was accompanied by a decrease in the
number of eggs, initially numerous in cyclostomes. It is dif-
fi cult to say whether this decrease was the consequence of
oocyte enlargement during transition to a non-feeding larva,
or suppression of oogonial division in the ovary during the
shift to intraovarian embryogenesis, or both. In the former
case, viviparity could result from a stepwise change from
simple to complex forms of embryonic incubation accompa-
nied by gradual increase in the amount of reserves in the
oocytes and reduction in their numbers (as in gymnolae-
mates). In the latter case, early onset of oocyte division in the
ovary would have also resulted in a reduction in oocyte num-
ber. Actually, both mechanisms could have been involved,
and subsequent evolution of matrotrophy might have pro-
moted a return to yolk-poor eggs. A transition from post-
ovulatory intracoelomic fertilization to an early intraovarian
mode could have induced the beginning of division directly
in the ovary.
If these assumptions are correct, then evolution of the
reproductive pattern in Cyclostomata could have followed
the same trajectory as the transition from reproductive pat-
tern II (as described for cheilostomes) to pattern III. A transi-
tion from pattern I is unlikely. In my opinion, the characteristic
set of “cyclostome” reproductive traits, involving intraovar-
ian embryogenesis and polyembryony, merits the status of a
separate reproductive pattern VI.
An embryo developing in the ovary could be provided
with additional nutrients; instead of forming new oocytes,
the ovary “feeds” a single embryo. Moreover, because the
cylindrical zooids of cyclostomes can elongate over an
extended period, the developing embryos would be afforded
more space relative to the brood chambers of gymnolae-
mates. Both of these factors could precondition the origin of
polyembryony in Cyclostomata. This event could have
3 Evolution of Reproductive Patterns in Cheilostomata
271
eventually resulted in the origin of specialized gonozooids
– infl ated voluminous chambers for embryonic incubation.
At the same time, the paleontological record contains indi-
cations that stenolaemates may have evolved polyembryony
much earlier. Buttler (
1991 ) suggested that the shape and
size of putative brood chambers in Cystoporata could indi-
cate polyembryony. McKinney ( 1981 ) found several colo-
nies of Permian fenestrates that were the product of fusion
of two individuals, each presumably originating from a
genetically identical larva, suggesting the existence of poly-
embryony (although the skeletal brood chambers of fenes-
trates are not very large). Pachut and Fisherkeller ( 2010 ),
however, have argued that polyembryony evolved only
once. At the same time, polyembryony, as well as endotro-
phy with brooding, could have evolved independently in dif-
ferent stenolaemate orders.
To note, polyembryony resulted in a reduction of the
number of reproducing zooids. Most cyclostome colonies
have only a single gonozooid (Borg 1926 ; Hayward and
Ryland 1985 ; Schäfer 1991 ; Ostrovsky and Taylor 1996 ;
Ostrovsky 1998a , b ), and all the free resources of the colony
are probably channelled towards its needs. Instead of form-
ing and supporting numerous small incubation chambers,
most of these bryozoans form a single one or just a few.
The above examples indicate that almost all variants of
embryonic incubation found in phylactolaemates, cyclo-
stomes and ctenostomes are either intracoelomic or intrazo-
oidal. In other words, it seems that the evolution of
incubation in these groups was predetermined by the
absence of structures that could be used for “constructing”
external brood chambers. Curiously, subsequent to the evo-
lution of external brooding in cheilostomes, there have been
multiple transitions to internal brooding in this order
(Ostrovsky et al. 2009c ).
It is important to stress here that extraembryonic nutrition
and placental analogues evolved in all bryozoan classes.
They are found in all living Cyclostomata and Phylactolaemata
as well as in many Ctenostomata and Cheilostomata.
Jablonski et al. ( 1997 ) posited that Taylor’s ( 1988a )
hypothesis concerning the role of the endotrophic larva in
cheilostome evolution is contradicted by the fact that cyclo-
stome bryozoans, having acquired a gonozooid (and hence
an endotrophic larva) in the Late Triassic, later underwent
only a modest diversifi cation (see also Taylor and Larwood
1990 ; Lidgard et al. 1993 ). Nevertheless, judging from
published data (Taylor and Larwood 1990 ; Lidgard et al.
1993 ; Jablonski et al. 1997 ; McKinney et al. 1998 ; Sepkoski
et al. 2000 ), this diversifi cation was the most dramatic evo-
lutionary event in the whole history of the order. McKinney
and Taylor (
2001 ) showed that the rates of increase of taxo-
nomic diversity in the Cyclostomata and Cheilostomata in
the Late Cretaceous were similar. In the opinion of Taylor
and Larwood ( 1990 ), there were three major radiations in
the history of the phylum – in the Ordovician (Stenolaemata),
the Middle Mesozoic (Cyclostomata) and the Late
Mesozoic (Cheilostomata). These authors speculated that
all three radiations may have been the consequence of the
origin of a lecithotrophic larva. As shown above, the origin
of structures for embryonic incubation (both putative and
real) is generally in concert with this hypothesis, however
our present knowledge is not suffi cient to venture any fur-
ther guesses.
3.6 Conclusion
Several reproductive patterns evolved during the history of
the bryozoan order Cheilostomata. The transition from
planktotrophy to lecithotrophy (from pattern I to pattern II)
was based on modifi cation of oogenesis, expressed in
increased oocyte size resulting from accumulation of
more nutrients. Additional consequences of this transition
were a decrease in the number of maturing oocytes formed
by a zooid, a shift to sequential (asynchronous) maturation, a
change in ovarian structure and a change in larval structure
and life span.
The structure of the brood chambers shows that within
this order parental care evolved independently during the rise
of the families Aeteidae, Scrupariidae (possibly twice),
Calloporidae, Tendridae, Thalamoporellidae and Alysidiidae
as well as in “ Carbasea ” indivisa and Bellulopora . This
means that suborder Flustrina is not monophyletic. Since
there are no known cheilostomes combining both the broad-
casting reproductive pattern and non-feeding larva, in all of
the above examples their ancestors should be non-brooding
malacostegans with a planktotrophic larva (or possibly a
ctenostome in the case of Aeteidae). Thus, lecithotrophy also
evolved in the Cheilostomata numerous times. Accordingly,
three new suborders Tendrina, Thalamoporellina and
Belluloporina have been newly introduced herein. Alysidiidae
and “ C .” indivisa most likely deserve the same treatment.
The evolution of brooding always accompanied a shift to
lecithotrophy, possibly compensating for the reduction in the
number of offspring. Some of the groups later independently
evolved extraembryonic nutrition, which also entailed modi-
fi cation of oogenesis, shifting from pattern II to pattern IV
and the latter to pattern III. Additionally, the transition from
intracoelomic to early intraovarian fertilization took place,
becoming the trigger for vitellogenesis. The acquisition of
nurse cells may have been the consequence of a transition to
early syngamy, which precluded the completion of oogonial
cytokinesis.
Brood chambers evolved in Cheilostomata repeatedly, on
the basis of modifi cations to spines, kenozooids, outgrowths
(outfolds) of the zooidal wall or the fertilization envelope. In
almost all cheilostome ovicells ooecia are not heterozooids
3.6 Conclusion
272
but body-wall outfolds. Ovicells with complete ooecia
originated by means of reduction in the number of spines
and their fl attening, the development of a proximally con-
cave spine arrangement, the loss of articulation of spines
from the gymnocyst, and the fusion of spines. Further modi-
fi cation of ovicells was closely connected with the evolution
of complex frontal shields. Reconstruction of the stages of
ovicell evolution provides further evidence for polyphyly of
lepraliomorph cheilostomes.
The main trends in the evolution of brooding structures in
the Cheilostomata were: (1) integration of zooids forming
the ovicell, (2) reduced ectooecial calcifi cation, (3) reduction
of the distal ooecium-producing zooid, (4) immersion of the
brood cavity with reduction of the ooecium and, as a conse-
quence, the origin of internal brood sacs, (5) a change in the
method of ovicell closure, and (6) the origin of peristomial
ovicells. In many cheilostome families these changes were
independent.
Cheilostome evolution was accompanied by progressive
increases in colonial integration, one of the key factors in the
success of the order. Integration was expressed as corre-
sponding changes in the sexual structure of the colony, in
synchronous maturation and spawning of gametes, sexual
zooidal polymorphism, and brooding in morphofunctional
modules (including ovicells). Sexual polymorphs and varied
sex-related structures in the colony were acquired repeatedly
in different cheilostome groups.
Importantly, the evolution of sexual reproduction in
Cheilostomata and Ctenostomata had similar trends, and
instances of parallelism abound. Viviparity evolved indepen-
dently in the order Cyclostomata (class Stenolaemata) and
the family Epistomiidae (order Cheilostomata).
In the Mesozoic and the Tertiary cheilostome evolution was
accompanied by the appearance of novelties facilitating or
enhancing responses to environmental change. The highest
plasticity, expressed in the acquisition of effective means of
protection (spines, brood chambers, zooidal polymorphs, fron-
tal shields), various growth forms and constructions of colo-
nies, new reproductive patterns and larval types, as well as high
colonial integration and modular complexity, allowed cheilo-
stomes to compete successfully with other epibionts, making
this order one of the most successful groups of colonial inver-
tebrates. Generally, many of these novelties independently
evolved in other bryozoan clades as well, helping bryozoans to
survive mass extinctions and to remain a dominant group in
most benthic assemblages for over 450 million years.
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3 Evolution of Reproductive Patterns in Cheilostomata
