267
have impacted the biota. Vertical transfer of water masses
caused by changes in their temperature and salinity inevitably 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 completely dependent on currents (Shanks 1995 ), could have
been eliminated in the open ocean, being unable to settle in
suitable sites (Mileikovsky 1971 ). Bryozoans with shortlived larvae would have had an evolutionary advantage in
this situation.
A number of gymnolaemate bryozoans retained planktotrophic 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 byproduct 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 million years) (see also Taylor and Larwood 1990 ). These rates
as well as the number of taxa (both brooding and broadcasting) 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 cation rates of cheilostomes have been decreasing, demonstrating, 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 lecithotrophy, once acquired, have sustained high speciation rates
for so long? The above authors put forward their own hypothesis, according to which the progressive radiation of cheilostome bryozoans was based on the evolution of new types of
protective skeletal frontal shields. The evolution of lecithotrophic larvae and brooding can be considered as a trigger
of radiation, later sustained by the evolution of skeletal structures. Boardman and Cheetham ( 1973 ) and Cheetham and
Cook ( 1983 ) considered as a key factor in the success of
Cheilostomata a combination of increased colonial integration, plasticity of different characters and evolution of complex 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 contributed considerably to success (McKinney 1986a , b ; McKinney
and Jackson 1989 ). Among other possible factors, the evolution 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 various forms of zooids but also extrazooidal units, frequently
spines, that themselves can be adapted for various functionalities. In fact, each ascophoran zooid is a construction consisting 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 constructions even more complex. The various permutations and
combinations of cormidial elements have been a major factor
in the diversifi cation and evolutionary success of cheilostomes, 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 primitive spinocyst and ooecium became the basis for evolutionary more advanced and reliable protective structures.
Increased phytoplankton abundance in combination with
sea-level rise, geographic isolation and other biotic and abiotic 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
have impacted the biota. Vertical transfer of water masses
caused by changes in their temperature and salinity inevitably 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 completely dependent on currents (Shanks 1995 ), could have
been eliminated in the open ocean, being unable to settle in
suitable sites (Mileikovsky 1971 ). Bryozoans with shortlived larvae would have had an evolutionary advantage in
this situation.
A number of gymnolaemate bryozoans retained planktotrophic 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 byproduct 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 million years) (see also Taylor and Larwood 1990 ). These rates
as well as the number of taxa (both brooding and broadcasting) 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 cation rates of cheilostomes have been decreasing, demonstrating, 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 lecithotrophy, once acquired, have sustained high speciation rates
for so long? The above authors put forward their own hypothesis, according to which the progressive radiation of cheilostome bryozoans was based on the evolution of new types of
protective skeletal frontal shields. The evolution of lecithotrophic larvae and brooding can be considered as a trigger
of radiation, later sustained by the evolution of skeletal structures. Boardman and Cheetham ( 1973 ) and Cheetham and
Cook ( 1983 ) considered as a key factor in the success of
Cheilostomata a combination of increased colonial integration, plasticity of different characters and evolution of complex 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 contributed considerably to success (McKinney 1986a , b ; McKinney
and Jackson 1989 ). Among other possible factors, the evolution 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 various forms of zooids but also extrazooidal units, frequently
spines, that themselves can be adapted for various functionalities. In fact, each ascophoran zooid is a construction consisting 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 constructions even more complex. The various permutations and
combinations of cormidial elements have been a major factor
in the diversifi cation and evolutionary success of cheilostomes, 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 primitive spinocyst and ooecium became the basis for evolutionary more advanced and reliable protective structures.
Increased phytoplankton abundance in combination with
sea-level rise, geographic isolation and other biotic and abiotic 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