58
( Bugula , Bicellariella ), Beaniidae ( Beania ), Epistomiidae
( Synnotum , Epistomia ), Candidae ( Scrupocellaria ), Cellariidae
( Cellaria ), Catenicellidae ( Catenicella ), Hippothoidae
( Celleporella ), Adeonidae ( Adeona , Adeonellopsis , Adeonella ,
Laminopora ), Hippopodinidae ( Hippopodina ), Poricellariidae
( Poricellaria ), Watersiporidae ( Watersipora ) and Calloporidae
( Crassimarginatella ).
A substantial increase in embryo size, sometimes accompanied by changes in the wall thickness of the brood chamber
(introvert), has been reported in eight brooding species of
Ctenostomata, in the families Flustrellidridae ( Flustrellidra ),
Sundanellidae ( Sundanella ), Nolellidae ( Nolella ), Walkeriidae
( Walkeria ), Mimosellidae ( Bantariella ), and Vesiculariidae
( Zoobotryon ) (Joliet 1877 ; Hincks 1880 ; Prouho 1892 ; Pace
1906 ; Waters 1914 ; Braem 1940 ; Silén 1942 , 1944 ; Banta
1968 ). This suggests that they exhibit EEN. Ultrastructural
studies of Zoobotryon verticillatum have also demonstrated
EEN in this species (Ostrovsky and Schwaha 2011 ). The
structure of the “ectodermic cushion” in the embryo sac of the
“protoctenostome” Labiostomella gisleni (Labiostomellidae)
(see Silén 1944 ) suggests that it, too, could be a placental
analogue.
The recent studies of cheilostome reproductive patterns
by Ostrovsky et al. ( 2009a ), Moosbrugger et al. ( 2012 ) and
Ostrovsky ( 2013 ) have revealed matrotrophic characters in
species of Bugulidae ( Bugula, Bicellariella ), Beaniidae
( Beania ),
Flustridae
( Gregarinidra ,
Klugefl ustra ,
Isosecurifl ustra ), Cellariidae ( Cellaria ), Microporidae
( Micropora ), Cribrilinidae ( Figularia ), Catenicellidae
( Cribricellina , Costaticella , Pterocella ), Hippothoidae
( Celleporella ), Watersiporidae ( Watersipora ), Myriaporidae
( Myriapora ), Urceoliporidae ( Urceolipora , Reciprocus ) and
Lanceoporidae (“ Calyptotheca” variolosa ), and an additional matrotrophic species of Mollia (Microporidae) has
been found (see Sects. 1.2.5 and 1.2.6 ).
As is clearly evident from a detailed analysis of the literature and my more recent studies, although embryo incubation accompanied by EEN has generally been considered a
rare mode of parental care in Gymnolaemata, it is in fact
quite common. We now have both direct and indirect
evidence from 39 genera in 26 families. Additional indirect
evidence suggests more examples, and this is very probable
since reproduction has been studied anatomically in less than
30% of all cheilostome families. For instance, embryo
enlargement is evident in an illustration of Harmeria scutulata (Cryptosulidae) (Kuklinski and Taylor 2006 ). The
above-mentioned family- level taxa (those examined directly
by the author and those inferred from the literature) represent
almost half of all gymnolaemate superfamilies. When
included with the wholly matrotrophic classes Stenolaemata
and Phylactolaemata, the wide distribution of EEN within
Bryozoa ranks it among the “most matrotrophic” invertebrate phyla, along with Arthropoda and Platyhelminthes.
1.3.5.2 Summary of Evidence of the Nutritive
Function of the Embryophore
Apart from embryo enlargement (which can be relatively small
in some species), the nutritive function of the embryophore
is confi rmed by the notable changes in cell morphology.
As shown above, these cells exhibit signifi cant shifts in size
and often color (in histological preparations) during incubation. These changes are suggestive of nutrient synthesis and/or
transport in relation to the embryo. A possible “excretory function” for the embryophore, implying bidirectional transport
(Woollacott and Zimmer 1975 ), should also be considered. It is
also clear that activation and functioning of the placental analogue is accompanied by proliferation of both epithelial and
funicular cells of the embryophore in some species, for example Gregarinidra serrata (Fig. 1.17 ) and Celleporella hyalina
(compare Figs. 1.26E and 1.27D ) (see also Woollacott and
Zimmer 1975 ). The expansion of “funicular tissue” during
incubation is especially impressive in Celleporella hyalina and
catenicellids of the genus Costaticella .
Increased physiological activity in embryophore cells is
also supported by cytological and ultrastructural evidence. In
Bugula neritina , Woollacott and Zimmer ( 1972a , b , 1975 )
described and illustrated large dark granules that accumulate
in the funicular cells adjoining the basal parts of the epithelial cells, and also in the epithelial cells themselves. My anatomical observations confi rm theirs. Moreover, in two other
species that brood their embryos inside internal sacs ( Beania
bilaminata and Reciprocus regalis ), similar granules were
concentrated exclusively in the apical parts of the epithelial
cells of the embryophore adjoining the embryo. Small dark
granules were found in these cells in “Calyptotheca” variolosa and Watersipora subtorquata , as well as co-occurring
with large pale vacuoles in the epithelial cells of Beania
bilaminata, Reciprocus regalis and Myriapora truncata .
Woollacott and Zimmer ( 1975 ) presented ultrastructural
evidence for EEN in Bugula neritina . The apical parts of
embryophore epithelial cells have numerous microvilli and
secretory vesicles, whereas adjoining embryonic cells form
numerous “deep infoldings,” indicating the existence of both
exo- and endocytosis. Confi rming the above-mentioned data,
the recent TEM-study of Bicellariella ciliata (see
Moosbrugger et al. 2012 ) showed that membranous infoldings of embryo cells are formed all over the embryo and are
not restricted to the area adjacent to the embryophore as
stated by Woollacott and Zimmer ( 1975 ). Microvilli surrounding the basal parts of larval cilia are suggestive of
active pinocytosis of brood-cavity fl uid in Celleporella hyalina , as described by Hughes ( 1987 ). Interestingly, cuticle
does not appear to be a barrier to reciprocal embryophore–
brood-cavity transport of low-molecular substances
(Woollacott and Zimmer 1975 ; Hughes 1987 ). Such nutrient
transfer through the cuticle of the maternal body wall is otherwise known only in crustaceans (Hoese and Janssen 1989 ).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
( Bugula , Bicellariella ), Beaniidae ( Beania ), Epistomiidae
( Synnotum , Epistomia ), Candidae ( Scrupocellaria ), Cellariidae
( Cellaria ), Catenicellidae ( Catenicella ), Hippothoidae
( Celleporella ), Adeonidae ( Adeona , Adeonellopsis , Adeonella ,
Laminopora ), Hippopodinidae ( Hippopodina ), Poricellariidae
( Poricellaria ), Watersiporidae ( Watersipora ) and Calloporidae
( Crassimarginatella ).
A substantial increase in embryo size, sometimes accompanied by changes in the wall thickness of the brood chamber
(introvert), has been reported in eight brooding species of
Ctenostomata, in the families Flustrellidridae ( Flustrellidra ),
Sundanellidae ( Sundanella ), Nolellidae ( Nolella ), Walkeriidae
( Walkeria ), Mimosellidae ( Bantariella ), and Vesiculariidae
( Zoobotryon ) (Joliet 1877 ; Hincks 1880 ; Prouho 1892 ; Pace
1906 ; Waters 1914 ; Braem 1940 ; Silén 1942 , 1944 ; Banta
1968 ). This suggests that they exhibit EEN. Ultrastructural
studies of Zoobotryon verticillatum have also demonstrated
EEN in this species (Ostrovsky and Schwaha 2011 ). The
structure of the “ectodermic cushion” in the embryo sac of the
“protoctenostome” Labiostomella gisleni (Labiostomellidae)
(see Silén 1944 ) suggests that it, too, could be a placental
analogue.
The recent studies of cheilostome reproductive patterns
by Ostrovsky et al. ( 2009a ), Moosbrugger et al. ( 2012 ) and
Ostrovsky ( 2013 ) have revealed matrotrophic characters in
species of Bugulidae ( Bugula, Bicellariella ), Beaniidae
( Beania ),
Flustridae
( Gregarinidra ,
Klugefl ustra ,
Isosecurifl ustra ), Cellariidae ( Cellaria ), Microporidae
( Micropora ), Cribrilinidae ( Figularia ), Catenicellidae
( Cribricellina , Costaticella , Pterocella ), Hippothoidae
( Celleporella ), Watersiporidae ( Watersipora ), Myriaporidae
( Myriapora ), Urceoliporidae ( Urceolipora , Reciprocus ) and
Lanceoporidae (“ Calyptotheca” variolosa ), and an additional matrotrophic species of Mollia (Microporidae) has
been found (see Sects. 1.2.5 and 1.2.6 ).
As is clearly evident from a detailed analysis of the literature and my more recent studies, although embryo incubation accompanied by EEN has generally been considered a
rare mode of parental care in Gymnolaemata, it is in fact
quite common. We now have both direct and indirect
evidence from 39 genera in 26 families. Additional indirect
evidence suggests more examples, and this is very probable
since reproduction has been studied anatomically in less than
30% of all cheilostome families. For instance, embryo
enlargement is evident in an illustration of Harmeria scutulata (Cryptosulidae) (Kuklinski and Taylor 2006 ). The
above-mentioned family- level taxa (those examined directly
by the author and those inferred from the literature) represent
almost half of all gymnolaemate superfamilies. When
included with the wholly matrotrophic classes Stenolaemata
and Phylactolaemata, the wide distribution of EEN within
Bryozoa ranks it among the “most matrotrophic” invertebrate phyla, along with Arthropoda and Platyhelminthes.
1.3.5.2 Summary of Evidence of the Nutritive
Function of the Embryophore
Apart from embryo enlargement (which can be relatively small
in some species), the nutritive function of the embryophore
is confi rmed by the notable changes in cell morphology.
As shown above, these cells exhibit signifi cant shifts in size
and often color (in histological preparations) during incubation. These changes are suggestive of nutrient synthesis and/or
transport in relation to the embryo. A possible “excretory function” for the embryophore, implying bidirectional transport
(Woollacott and Zimmer 1975 ), should also be considered. It is
also clear that activation and functioning of the placental analogue is accompanied by proliferation of both epithelial and
funicular cells of the embryophore in some species, for example Gregarinidra serrata (Fig. 1.17 ) and Celleporella hyalina
(compare Figs. 1.26E and 1.27D ) (see also Woollacott and
Zimmer 1975 ). The expansion of “funicular tissue” during
incubation is especially impressive in Celleporella hyalina and
catenicellids of the genus Costaticella .
Increased physiological activity in embryophore cells is
also supported by cytological and ultrastructural evidence. In
Bugula neritina , Woollacott and Zimmer ( 1972a , b , 1975 )
described and illustrated large dark granules that accumulate
in the funicular cells adjoining the basal parts of the epithelial cells, and also in the epithelial cells themselves. My anatomical observations confi rm theirs. Moreover, in two other
species that brood their embryos inside internal sacs ( Beania
bilaminata and Reciprocus regalis ), similar granules were
concentrated exclusively in the apical parts of the epithelial
cells of the embryophore adjoining the embryo. Small dark
granules were found in these cells in “Calyptotheca” variolosa and Watersipora subtorquata , as well as co-occurring
with large pale vacuoles in the epithelial cells of Beania
bilaminata, Reciprocus regalis and Myriapora truncata .
Woollacott and Zimmer ( 1975 ) presented ultrastructural
evidence for EEN in Bugula neritina . The apical parts of
embryophore epithelial cells have numerous microvilli and
secretory vesicles, whereas adjoining embryonic cells form
numerous “deep infoldings,” indicating the existence of both
exo- and endocytosis. Confi rming the above-mentioned data,
the recent TEM-study of Bicellariella ciliata (see
Moosbrugger et al. 2012 ) showed that membranous infoldings of embryo cells are formed all over the embryo and are
not restricted to the area adjacent to the embryophore as
stated by Woollacott and Zimmer ( 1975 ). Microvilli surrounding the basal parts of larval cilia are suggestive of
active pinocytosis of brood-cavity fl uid in Celleporella hyalina , as described by Hughes ( 1987 ). Interestingly, cuticle
does not appear to be a barrier to reciprocal embryophore–
brood-cavity transport of low-molecular substances
(Woollacott and Zimmer 1975 ; Hughes 1987 ). Such nutrient
transfer through the cuticle of the maternal body wall is otherwise known only in crustaceans (Hoese and Janssen 1989 ).
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis