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 phytoplanktonic groups, which constitute the lion’s share of the bryozoan 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 silicofl 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 calcareous or siliceous skeletons. It is therefore all the noteworthy that the diversity of dinofl agellates (Dinofl agellata)
skyrocketed in the Albian (Martin 2003 ), when brooding
cheilostomes evolved. These unicellular organisms constitute 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 favourable for invertebrates with planktotrophic larvae (McEdward
and Miner 2003 ). However, such periods should be favourable not only for such larvae but also for adult fi lter-feeding
animals. Increased plankton abundance impacts the epibenthos, 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 component of many bottom communities, food has been experimentally 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 uence 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 cheilostomes and increasing phytoplankton diversity and abundance 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 bryozoans – 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 speciation. 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 facultative 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 origin of brood chambers. In addition, the transition to a shortlived endotrophic larva would also have been advantageous
against increasing predation pressure (see Nielsen 1998 ).
It should be emphasized that progressive colonial integration was a key to the success of Cheilostomata. They evolved
polymorphism (including sexual polymorphism) and brooding morphofunctional modules consisting of autozooids with
ovicells and avicularia (Lidgard et al. 2012 ). The broad distribution 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
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 phytoplanktonic groups, which constitute the lion’s share of the bryozoan 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 silicofl 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 calcareous or siliceous skeletons. It is therefore all the noteworthy that the diversity of dinofl agellates (Dinofl agellata)
skyrocketed in the Albian (Martin 2003 ), when brooding
cheilostomes evolved. These unicellular organisms constitute 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 favourable for invertebrates with planktotrophic larvae (McEdward
and Miner 2003 ). However, such periods should be favourable not only for such larvae but also for adult fi lter-feeding
animals. Increased plankton abundance impacts the epibenthos, 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 component of many bottom communities, food has been experimentally 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 uence 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 cheilostomes and increasing phytoplankton diversity and abundance 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 bryozoans – 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 speciation. 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 facultative 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 origin of brood chambers. In addition, the transition to a shortlived endotrophic larva would also have been advantageous
against increasing predation pressure (see Nielsen 1998 ).
It should be emphasized that progressive colonial integration was a key to the success of Cheilostomata. They evolved
polymorphism (including sexual polymorphism) and brooding morphofunctional modules consisting of autozooids with
ovicells and avicularia (Lidgard et al. 2012 ). The broad distribution 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