151
brooding and epistegal cavity in a Tendra -like ancestor.
Subsequent new data on ovicell structure in fossil calloporids, cribrimorphs and monoporellids have refuted this
hypothesis. Now we may be fairly sure that ooecia of the vast
majority of cheilostomes originated from the mural spines of
the proximal part of the distal autozooid in a calloporid
ancestor (see Sects. 2.3.1.1 and 2.4.3 ), whereas tendrid brood
chambers evolved independently (Ostrovsky and Taylor
2005a ; see also Silén 1944 ).
Spines (articulated or non-articulated) are common in
both fossil and Recent cheilostomes. Presumably they
originated as protective structures (Larwood and Taylor
1981 ; Taylor 1999 ). A protective function is evidenced not
only by their shape and position; it was experimentally
shown that the formation, increase in number and size of
spines (or spinules) may be induced by nudibranch predators, strong water turbulence or abrasion resulting from
frequent contact between a colony and neighbouring algal
thalli (Yoshioka 1982 ; Harvell 1984 , 1986 , 1992 ;
Whitehead et al. 1996 ; Bayer et al. 1997 ; reviewed in
McKinney et al. 2003 ).
Gymnolaemate spines are very varied, ranging from stout
hollow structures interpreted to be modifi ed zooids (kenozooids or spinozooids) to simple cuticular outgrowths of the
membranous body wall (Smitt 1868 , 1872 ; Nitsche 1871a , b ;
Calvet 1900 ; Levinsen 1909 ; Borg 1931 ; Cori 1941 ; Silén
1942 , 1944 , 1947 , 1977 ; Ryland 1979 , 1982 ; Harvell 1984 ,
1986 ). Whatever their origin, the spines/costae of all, but one
Recent cheilostomes that have been studied are outgrowths
of the zooidal body wall; there are no pore plates with specialized pore-cell complexes between hollow spines and the
visceral coelom (Silén 1947 ; Bobin 1968 ; Ostrovsky 1998 ).
In contrast, costae of Bellulopora bellula are supposedly true
kenozooids. They have a long strip of hypostegal coelom
confl uent with visceral coelom of autozooid via a communication pore with a cuticular annulus identical to communication pores of Cheilostomata.
2.4.3 Early Stages in Ovicell Evolution
The fact that mural spines are situated around the frontal
membrane indicates that their origin may have been associated with the protection of this most vulnerable part of the
zooidal surface. Later, the spines on the proximal gymnocyst
became specialized for the protection of the embryo.
Spinose and costate brood chambers are not uncommon
among Cheilostomata. They were widespread in the Late
Cretaceous (28 species). In the Cenozoic 19 other species are
known, 11 of them Recent. Spinose and costate brood chambers are found in the families Calloporidae ( Distelopora ,
Unidistelopora , Gilbertopora ; see Sect. 2.3.1 ), Monoporellidae ( Stichomicropora , Monoporella ), Macroporidae
( Macropora ), Cribrilinidae ( Leptocheilopora , Craticulacella ,
(?) Thoracopora ), Tendridae ( Tendra , Heteroecium ) and in
the genus Bellulopora (summarized in Ostrovsky and Taylor
2005a ). As for their geochronological distribution, the timelines are as follows: Calloporidae – Early Cenomanian to
Early Campanian; Monoporellidae – Early Cenomanian to
Recent; Macroporidae – Late Eocene to Recent; Cribrilinidae –
Early Cenomanian to Early Campanian; Bellulopora –
Pleistocene to Recent. Acanthostegal brood chambers are
known only in living bryozoans of the family Tendridae.
Importantly, the three oldest superfamilies of brooding cheilostomes (Calloporoidea, Microporoidea and Cribrilinoidea)
include Cenomanian species with primitive spinose or costate ovicells. Microporids and cribrimorphs are generally
considered as calloporid descendants (Gordon 2000 ).
The earliest ovicells are recorded in the calloporids
Wilbertopora and Marginaria from the Late Albian
(Cheetham 1954 , 1975 ; Taylor 1988 ; Cheetham et al. 2006 ).
Strikingly, species belonging to these genera have complete
ooecia (except for a medial suture in Wilbertopora ) and
appeared somewhat earlier in the geochronological record
than known calloporids with spinose ooecia. Nevertheless,
spinose ooecia are more primitive structurally, which indicates that they must have occurred in calloporids preceding
those with complete ooecia. Such forerunners need not have
occurred much earlier in time – it appears likely that the transition from spinose and costate ovicells to complete ooecia
was relatively fast in geological terms, corresponding to the
time gap between Wilbertopora (the earliest known cheilostome with ooecia) and Distelopora (the earliest cheilostome
with spinose ooecia) (see Ostrovsky and Taylor 2004 ),
i.e. about 10 million years.
As indicated, the main event in ovicell evolution was the
modifi cation of mural spines initially protecting the vulnerable membranous frontal wall of autozooids. A search for
the ancestors of the fi rst brooding cheilostomes leads us to
Early Cretaceous bryozoans similar to Spinicharixa (see
Taylor 1986 ). In this malacostegan genus ovicells are absent,
but the opesia is surrounded by the bases of articulated
spines. So, as in Recent malacostegans like Villicharixa strigosa (see Gordon 1989b ) (Fig. 2.53 ), the frontal membrane
in Spinicharixa and in the fi rst cheilostome brooders was
protected by a palisade of long spines. These spines also
presumably protected eggs laid on the frontal surface of the
distal zooid by the polypide of the maternal one. If the eggs
were surrounded by sticky fertilization envelopes (see Sect.
3.4.3 ), this could additionally prevent their removal from
the colony.
The fi rst step towards a specialized brood chamber was
bending or growth re-orientation of proximal spines towards
the opening of the maternal zooid (Fig. 2.54A ) (Ostrovsky and
Taylor 2004 , 2005a ). Spinose ovicells with the simplest morphology are found in the Late Cretaceous genera Distelopora
2.4 Evolution of Brood Chambers in Cheilostomata
brooding and epistegal cavity in a Tendra -like ancestor.
Subsequent new data on ovicell structure in fossil calloporids, cribrimorphs and monoporellids have refuted this
hypothesis. Now we may be fairly sure that ooecia of the vast
majority of cheilostomes originated from the mural spines of
the proximal part of the distal autozooid in a calloporid
ancestor (see Sects. 2.3.1.1 and 2.4.3 ), whereas tendrid brood
chambers evolved independently (Ostrovsky and Taylor
2005a ; see also Silén 1944 ).
Spines (articulated or non-articulated) are common in
both fossil and Recent cheilostomes. Presumably they
originated as protective structures (Larwood and Taylor
1981 ; Taylor 1999 ). A protective function is evidenced not
only by their shape and position; it was experimentally
shown that the formation, increase in number and size of
spines (or spinules) may be induced by nudibranch predators, strong water turbulence or abrasion resulting from
frequent contact between a colony and neighbouring algal
thalli (Yoshioka 1982 ; Harvell 1984 , 1986 , 1992 ;
Whitehead et al. 1996 ; Bayer et al. 1997 ; reviewed in
McKinney et al. 2003 ).
Gymnolaemate spines are very varied, ranging from stout
hollow structures interpreted to be modifi ed zooids (kenozooids or spinozooids) to simple cuticular outgrowths of the
membranous body wall (Smitt 1868 , 1872 ; Nitsche 1871a , b ;
Calvet 1900 ; Levinsen 1909 ; Borg 1931 ; Cori 1941 ; Silén
1942 , 1944 , 1947 , 1977 ; Ryland 1979 , 1982 ; Harvell 1984 ,
1986 ). Whatever their origin, the spines/costae of all, but one
Recent cheilostomes that have been studied are outgrowths
of the zooidal body wall; there are no pore plates with specialized pore-cell complexes between hollow spines and the
visceral coelom (Silén 1947 ; Bobin 1968 ; Ostrovsky 1998 ).
In contrast, costae of Bellulopora bellula are supposedly true
kenozooids. They have a long strip of hypostegal coelom
confl uent with visceral coelom of autozooid via a communication pore with a cuticular annulus identical to communication pores of Cheilostomata.
2.4.3 Early Stages in Ovicell Evolution
The fact that mural spines are situated around the frontal
membrane indicates that their origin may have been associated with the protection of this most vulnerable part of the
zooidal surface. Later, the spines on the proximal gymnocyst
became specialized for the protection of the embryo.
Spinose and costate brood chambers are not uncommon
among Cheilostomata. They were widespread in the Late
Cretaceous (28 species). In the Cenozoic 19 other species are
known, 11 of them Recent. Spinose and costate brood chambers are found in the families Calloporidae ( Distelopora ,
Unidistelopora , Gilbertopora ; see Sect. 2.3.1 ), Monoporellidae ( Stichomicropora , Monoporella ), Macroporidae
( Macropora ), Cribrilinidae ( Leptocheilopora , Craticulacella ,
(?) Thoracopora ), Tendridae ( Tendra , Heteroecium ) and in
the genus Bellulopora (summarized in Ostrovsky and Taylor
2005a ). As for their geochronological distribution, the timelines are as follows: Calloporidae – Early Cenomanian to
Early Campanian; Monoporellidae – Early Cenomanian to
Recent; Macroporidae – Late Eocene to Recent; Cribrilinidae –
Early Cenomanian to Early Campanian; Bellulopora –
Pleistocene to Recent. Acanthostegal brood chambers are
known only in living bryozoans of the family Tendridae.
Importantly, the three oldest superfamilies of brooding cheilostomes (Calloporoidea, Microporoidea and Cribrilinoidea)
include Cenomanian species with primitive spinose or costate ovicells. Microporids and cribrimorphs are generally
considered as calloporid descendants (Gordon 2000 ).
The earliest ovicells are recorded in the calloporids
Wilbertopora and Marginaria from the Late Albian
(Cheetham 1954 , 1975 ; Taylor 1988 ; Cheetham et al. 2006 ).
Strikingly, species belonging to these genera have complete
ooecia (except for a medial suture in Wilbertopora ) and
appeared somewhat earlier in the geochronological record
than known calloporids with spinose ooecia. Nevertheless,
spinose ooecia are more primitive structurally, which indicates that they must have occurred in calloporids preceding
those with complete ooecia. Such forerunners need not have
occurred much earlier in time – it appears likely that the transition from spinose and costate ovicells to complete ooecia
was relatively fast in geological terms, corresponding to the
time gap between Wilbertopora (the earliest known cheilostome with ooecia) and Distelopora (the earliest cheilostome
with spinose ooecia) (see Ostrovsky and Taylor 2004 ),
i.e. about 10 million years.
As indicated, the main event in ovicell evolution was the
modifi cation of mural spines initially protecting the vulnerable membranous frontal wall of autozooids. A search for
the ancestors of the fi rst brooding cheilostomes leads us to
Early Cretaceous bryozoans similar to Spinicharixa (see
Taylor 1986 ). In this malacostegan genus ovicells are absent,
but the opesia is surrounded by the bases of articulated
spines. So, as in Recent malacostegans like Villicharixa strigosa (see Gordon 1989b ) (Fig. 2.53 ), the frontal membrane
in Spinicharixa and in the fi rst cheilostome brooders was
protected by a palisade of long spines. These spines also
presumably protected eggs laid on the frontal surface of the
distal zooid by the polypide of the maternal one. If the eggs
were surrounded by sticky fertilization envelopes (see Sect.
3.4.3 ), this could additionally prevent their removal from
the colony.
The fi rst step towards a specialized brood chamber was
bending or growth re-orientation of proximal spines towards
the opening of the maternal zooid (Fig. 2.54A ) (Ostrovsky and
Taylor 2004 , 2005a ). Spinose ovicells with the simplest morphology are found in the Late Cretaceous genera Distelopora
2.4 Evolution of Brood Chambers in Cheilostomata