165
propinqua , Characodoma porcellanum and some others)
that the proximal position of the pore is combined with the
distal position of the ectooecium base, which appears to be
associated with the way in which the ovicell fl oor fuses with
the proximal area of the calcifi ed wall of the frontal shield.
At the same time, different combinations of proximal and
distal positions of the pore and ectooecial base can be found
in the same genus ( Porella , Rhamphostomella ) or family
(Bryocryptellidae, Smittinidae).
As for ovicellogenesis, in most species with the ectooecial base in a “distal” position (the plesiomorphic condition), the ooecial fold begins to form at the colony periphery
long before the frontal shield of the distal zooid is completed. In contrast, in species with the ooecial base proximal, the “double- disc” stage often develops from the edge
of the narrow membranous window (in fact, a membranecovered groove with a communication pore at the bottom;
see Sect. 2.3.2 ) after the distal zooid has been completed.
In this case, formation of the lepralielliform ooecium is not
connected with the formation of new zooids at the colony
periphery, and can be postponed. A similar correlation
exists in ascophorans with microporelliform ooecia (see
Sect. 2.3.2 ).
2.4.9 Brood Chambers in the Scrupariidae,
Thalamoporellidae and Alysidiidae
In ovicells with “bivalved” or “bilobate” (“bivalvular,”
“double- valved,” “two-valved,” see Levinsen 1902 , 1909 ;
Waters 1909 ; Hyman 1959 ) ooecia, the protective capsule is
constructed of two symmetrical halves. Such ovicells are
patchily distributed among the Cheilostomata, some of
which are closely related and some phylogenetically distant
(Calloporidae, Cribrilinidae, Euthyroididae, Scrupariidae,
Thalamoporellidae, Alysidiidae) (see also Sects. 2.3.1 , 2.3.2 ,
and 2.3.4 ).
In Scruparia , Brettiopsis , Alysidium and Catenicula , each
valve/plate is obviously kenozooidal (although anatomical
study is needed in all these cases), budded either from the maternal zooid or from each other, whereas in Thalamoporella they
are fused hollow outgrowths of the frontal surface around the
orifi ce of the maternal autozooid, a unique instance among cheilostomes. In contrast, in Wilbertopora , Gilbertopora , Bryocalyx ,
Valdemunitella , Euthyroides , Corbulipora , Puellina , Figularia ,
and Filaguria the ooecial halves are outgrowths of the distal
zooid – either an autozooid, an avicularium or a kenozooid.
A special type of brood chamber (synoecium) is found in
Catenicula that consists of eight fl attened elements (presumed
kenozooids) (O’Donoghue 1924 ; O’Donoghue and Watteville
1944 ). I additionally propose to designate the synoecium a
“multivalved brood chamber”.
Thus, bilobate ovicells are not homologous throughout
the Cheilostomata, supporting the hypothesis of independent
evolution of brooding (Taylor 1988 ; Ostrovsky and Taylor
2005a ; see also discussion in Santagata and Banta 1996 ).
Many other cheilostomes have a median suture in their ovicells (Ostrovsky 2002 ; Ostrovsky et al. 2009a ), but the use of
the term “bivalved” for them is less appropriate, since the
suture is normally short and often restricted to a part of the
ovicell roof (see Ostrovsky 1998 ).
Scruparia and Brettiopsis (Scrupariidae) have bivalved
terminal ovicells consisting of a pair of lobes, presumably
kenozooids. Appearing in the Maastrichtian, scrupariids
have traditionally been separated from the rest of the brooding cheilostomes owing to a set of morphological and anatomical differences. That embryo incubation in scrupariids
evolved independently of other cheilostomes was fi rst
suggested by Osburn ( 1950 ; see also Ryland 1974 ).
Waeschenbach et al. ( 2012 ) molecular analysis supports this
idea, with Scruparia nested among malacostegans in their
phylogeny (see also Sect. 3.4.1 ). In addition, species of
Scruparia have a setigerous collar (Prenant and Bobin 1966 ;
Banta et al. 1995 ) and brood several embryos simultaneously. Both of these characters, considered to be primitive,
are known in ctenostomes. Finally, the larva of Scruparia ,
illustrated by Barrois ( 1877 ), strongly resembles the larva of
the ctenostome Flustrellidra hispida (see Zimmer and
Woollacott 1977 ).
Alysidium has bivalved brood chambers with a similar
structure but the valves are connected to the maternal zooid
by a cuticular base that permits them to bend outwards.
This difference and zooid structure mediate against a relationship with Scruparia . The Alysidiidae also includes
Catenicula but it is unclear if its multivalved brood chamber is homologous to that of Alysidium . Levinsen ( 1909 )
interpreted the ooecial valves of Alysidium to be modifi ed
autozooids. The coelomic cavity of the valve (kenozooid) is
separated from the visceral coelom by a pore plate. In other
words, alysidiid ovicells also appear to have evolved independently of other cheilostomes. Unfortunately, this conclusion sheds little light upon the phylogenetic connections
of this family, which may well turn out to be unrelated to
the other Flustrina.
The origin of brooding in the Thalamoporellidae is a
complicated and essentially unresolved question. This is
partly because of a lack of information about the structure of
the brood chamber as well as the uncertain position of the
family in cheilostome classifi cation. Harmer ( 1926 , pp. 291,
293–294) regarded the bilobate ovicells of Thalamoporella
as non-homologous to the ovicells of other cheilostomes
(see also Ryland 1974 ), being “modifi cations of the adoral
tubercles … borne by the ordinary zooecia”. Specifi cally,
the ooecial lobes are not kenozooids, as in Scruparia and
2.4 Evolution of Brood Chambers in Cheilostomata
propinqua , Characodoma porcellanum and some others)
that the proximal position of the pore is combined with the
distal position of the ectooecium base, which appears to be
associated with the way in which the ovicell fl oor fuses with
the proximal area of the calcifi ed wall of the frontal shield.
At the same time, different combinations of proximal and
distal positions of the pore and ectooecial base can be found
in the same genus ( Porella , Rhamphostomella ) or family
(Bryocryptellidae, Smittinidae).
As for ovicellogenesis, in most species with the ectooecial base in a “distal” position (the plesiomorphic condition), the ooecial fold begins to form at the colony periphery
long before the frontal shield of the distal zooid is completed. In contrast, in species with the ooecial base proximal, the “double- disc” stage often develops from the edge
of the narrow membranous window (in fact, a membranecovered groove with a communication pore at the bottom;
see Sect. 2.3.2 ) after the distal zooid has been completed.
In this case, formation of the lepralielliform ooecium is not
connected with the formation of new zooids at the colony
periphery, and can be postponed. A similar correlation
exists in ascophorans with microporelliform ooecia (see
Sect. 2.3.2 ).
2.4.9 Brood Chambers in the Scrupariidae,
Thalamoporellidae and Alysidiidae
In ovicells with “bivalved” or “bilobate” (“bivalvular,”
“double- valved,” “two-valved,” see Levinsen 1902 , 1909 ;
Waters 1909 ; Hyman 1959 ) ooecia, the protective capsule is
constructed of two symmetrical halves. Such ovicells are
patchily distributed among the Cheilostomata, some of
which are closely related and some phylogenetically distant
(Calloporidae, Cribrilinidae, Euthyroididae, Scrupariidae,
Thalamoporellidae, Alysidiidae) (see also Sects. 2.3.1 , 2.3.2 ,
and 2.3.4 ).
In Scruparia , Brettiopsis , Alysidium and Catenicula , each
valve/plate is obviously kenozooidal (although anatomical
study is needed in all these cases), budded either from the maternal zooid or from each other, whereas in Thalamoporella they
are fused hollow outgrowths of the frontal surface around the
orifi ce of the maternal autozooid, a unique instance among cheilostomes. In contrast, in Wilbertopora , Gilbertopora , Bryocalyx ,
Valdemunitella , Euthyroides , Corbulipora , Puellina , Figularia ,
and Filaguria the ooecial halves are outgrowths of the distal
zooid – either an autozooid, an avicularium or a kenozooid.
A special type of brood chamber (synoecium) is found in
Catenicula that consists of eight fl attened elements (presumed
kenozooids) (O’Donoghue 1924 ; O’Donoghue and Watteville
1944 ). I additionally propose to designate the synoecium a
“multivalved brood chamber”.
Thus, bilobate ovicells are not homologous throughout
the Cheilostomata, supporting the hypothesis of independent
evolution of brooding (Taylor 1988 ; Ostrovsky and Taylor
2005a ; see also discussion in Santagata and Banta 1996 ).
Many other cheilostomes have a median suture in their ovicells (Ostrovsky 2002 ; Ostrovsky et al. 2009a ), but the use of
the term “bivalved” for them is less appropriate, since the
suture is normally short and often restricted to a part of the
ovicell roof (see Ostrovsky 1998 ).
Scruparia and Brettiopsis (Scrupariidae) have bivalved
terminal ovicells consisting of a pair of lobes, presumably
kenozooids. Appearing in the Maastrichtian, scrupariids
have traditionally been separated from the rest of the brooding cheilostomes owing to a set of morphological and anatomical differences. That embryo incubation in scrupariids
evolved independently of other cheilostomes was fi rst
suggested by Osburn ( 1950 ; see also Ryland 1974 ).
Waeschenbach et al. ( 2012 ) molecular analysis supports this
idea, with Scruparia nested among malacostegans in their
phylogeny (see also Sect. 3.4.1 ). In addition, species of
Scruparia have a setigerous collar (Prenant and Bobin 1966 ;
Banta et al. 1995 ) and brood several embryos simultaneously. Both of these characters, considered to be primitive,
are known in ctenostomes. Finally, the larva of Scruparia ,
illustrated by Barrois ( 1877 ), strongly resembles the larva of
the ctenostome Flustrellidra hispida (see Zimmer and
Woollacott 1977 ).
Alysidium has bivalved brood chambers with a similar
structure but the valves are connected to the maternal zooid
by a cuticular base that permits them to bend outwards.
This difference and zooid structure mediate against a relationship with Scruparia . The Alysidiidae also includes
Catenicula but it is unclear if its multivalved brood chamber is homologous to that of Alysidium . Levinsen ( 1909 )
interpreted the ooecial valves of Alysidium to be modifi ed
autozooids. The coelomic cavity of the valve (kenozooid) is
separated from the visceral coelom by a pore plate. In other
words, alysidiid ovicells also appear to have evolved independently of other cheilostomes. Unfortunately, this conclusion sheds little light upon the phylogenetic connections
of this family, which may well turn out to be unrelated to
the other Flustrina.
The origin of brooding in the Thalamoporellidae is a
complicated and essentially unresolved question. This is
partly because of a lack of information about the structure of
the brood chamber as well as the uncertain position of the
family in cheilostome classifi cation. Harmer ( 1926 , pp. 291,
293–294) regarded the bilobate ovicells of Thalamoporella
as non-homologous to the ovicells of other cheilostomes
(see also Ryland 1974 ), being “modifi cations of the adoral
tubercles … borne by the ordinary zooecia”. Specifi cally,
the ooecial lobes are not kenozooids, as in Scruparia and
2.4 Evolution of Brood Chambers in Cheilostomata