56
cytoplasmic zone of mature nurse cells, which may indicate
a change in the character of synthetic activity of these cells at
different stages.
The increase in cell volume of oocytes is much greater
than that of the nucleus. In nurse cells, on the other hand, the
nucleus enlarges almost as much as the cell itself (see
Tables 1.4 , 1.5 , 1.6 and 1.7 ), which may point to a leading
role for the nucleus in the formation of components involved
in protein synthesis for the oocyte. The nurse cell itself,
while actively synthesizing, barely grows, which must mean
that the substances formed in it are transported to the oocyte.
The evolutionary advantage of such an intimate relationship as partial or complete fusion of oocytes and nurse cells
is apparent, since substances and/or organelles synthesized
by the one can be easily transported into the cytoplasm of
the other. Among other invertebrates, intercellular transport
and phagocytosis of “nurse cells” by oocytes is known in
some sponges and coelenterates as well as several species of
annelids and crustaceans (Adiyodi and Adiyodi 1983 ;
Wourms 1987 ). My data provide evidence that, at later
growth stages of the oocyte doublet, contact between siblings may become greater, at least in some species. It is no
longer a narrow cytoplasmic bridge but a relatively broad
zone of common cytoplasm (Figs. 1.7C and 1.13B ). The
nurse cell separates from the mature oocyte at ovulation.
In Callopora lineata , as the nurse separates, it takes with it
some yolk granules from the cytoplasm of the oocyte
(Fig. 1.6D ). It is unlikely they are formed in the nurse cell as
they are much larger than its usual inclusions.
1.3.5 Matrotrophic Brooding
Extraembryonic nutrition (EEN) or matrotrophy is the direct
parental provisioning of an embryo with nutrients during
incubation. This is one of the most effective modes of parental
care, evolving independently in more than half of all metazoan
phyla, including Porifera, Cnidaria, Platyhelminthes and
Nematoda (both free-living and parasitic), Nemertea,
Annelida, Mollusca, Bryozoa, Kamptozoa, Arthropoda,
Onychophora, Echinodermata, Chordata and some other
groups (see Giese and Pearse 1974 , 1975a , b , 1977 ; Giese
et al. 1979 , 1991 ; Adiyodi and Adiyodi 1989 , 1990 ; Blackburn
2005a ; Wourms et al. 1988 ; Batygina et al. 2006 ; and references therein). The simplest mode of matrotrophy is histotrophy, that is, absorption via embryonic epithelium, whereas
the most complex is placentotrophy, which, according to
Mossman’s ( 1937 , p. 156) widely accepted defi nition of a
placenta, involves “any intimate apposition or fusion of the
fetal organs to the maternal [or paternal] tissues for physiological exchange”. In addition to therian mammals, placentas
are widely documented among squamate reptiles, fi shes
(reviewed in Wourms 1981 ; Wourms et al. 1988 ; Wourms and
Lombardi 1992 ; Blackburn 1992 , 1993 , 1999 , 2005a , b ;
Blackburn et al. 1985 ; Wooding and Burton 2008 ) and invertebrates, being often referred to as placental analogues or
sometimes pseudoplacentas (Turner 1940 ; Hagan 1951 ;
Blackburn 1999 ; Farley 1996 ). Despite the two latter terms
being considered archaic, “placental analogue” still seems
suitable for describing the simplest placentas of some invertebrates. The main reason for this is that close apposition
between the embryo and the nutritive organ or tissue is often
established during the later stages of incubation. Prior to this,
the embryo grows suspended in a brood cavity without any
contact with the maternal wall that provides nutrition, absorbing nutrients from the surrounding fl uid of the incubation
chamber. Thus, there is matrotrophic nutrition, but not placentation in the strict sense during much of the incubation
period (Ostrovsky 2013 ).
In most groups including species with EEN, the majority
of species are either egg-laying or non-matrotrophic livebearing animals. Known exceptions are trematodes
(Platyhelminthes), the arthropod orders Scorpiones,
Pseudoscorpiones and Strepsiptera, and salps and mammals
among chordates. All species in these groups have EEN
(Hagan 1951 ; Weygoldt 1969 ; Francke 1982 ; Godeaux 1990 ;
Lombardi 1998 ; Galaktionov and Dobrovolskij 2003 ;
Blackburn 2005a ). Phylum Bryozoa is another example, in
which all living representatives of the classes Stenolaemata
and Phylactolaemata and many species from the class
Gymnolaemata are known or inferred to be matrotrophic
(Ostrovsky 2009 ; Ostrovsky et al. 2009a ). Moreover, in contrast with the vast majority of matrotrophic animals that are
viviparous, many matrotrophic bryozoans are brooders and
incubate their embryos outside the parental body cavity.
Apart from the Pseudoscorpionida and Salpida, matrotrophic
brooding is generally regarded as rare and is known in several
chordates (ascidians, bony fi shes and amphibians), a handful
of bivalve and gastropod molluscs, and a few crustaceans,
kamptozoans and echinoderms (Mukai et al. 1987 ; Hoese
and Janssen 1989 ; Nielsen 1990 ; Warburg and Rosenberg
1996 ; Lombardi 1998 ; Schwartz and Dimock 2001 ;
Korniushin and Glaubrecht 2003 ; O’Loughlin et al. 2009 ).
1.3.5.1 Historical Overview
Extant species from the viviparous order Cyclostomata (class
Stenolaemata) and the brooding class Phylactolaemata are
all matrotrophic. It has long been known that their embryos
enlarge during incubation and the anatomy of supposed
placental analogues has been described (Harmer 1893 ;
Braem 1897 , 1908 ; Borg 1926 ; Brien 1953 ).
In contrast, EEN was until recently considered to be rare
in gymnolaemates. There are relatively few records in the
historical literature, citing such features as embryonic
enlargement during incubation and hypertrophied epithelial
walls in brood chambers. Although providing evidence for
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis
cytoplasmic zone of mature nurse cells, which may indicate
a change in the character of synthetic activity of these cells at
different stages.
The increase in cell volume of oocytes is much greater
than that of the nucleus. In nurse cells, on the other hand, the
nucleus enlarges almost as much as the cell itself (see
Tables 1.4 , 1.5 , 1.6 and 1.7 ), which may point to a leading
role for the nucleus in the formation of components involved
in protein synthesis for the oocyte. The nurse cell itself,
while actively synthesizing, barely grows, which must mean
that the substances formed in it are transported to the oocyte.
The evolutionary advantage of such an intimate relationship as partial or complete fusion of oocytes and nurse cells
is apparent, since substances and/or organelles synthesized
by the one can be easily transported into the cytoplasm of
the other. Among other invertebrates, intercellular transport
and phagocytosis of “nurse cells” by oocytes is known in
some sponges and coelenterates as well as several species of
annelids and crustaceans (Adiyodi and Adiyodi 1983 ;
Wourms 1987 ). My data provide evidence that, at later
growth stages of the oocyte doublet, contact between siblings may become greater, at least in some species. It is no
longer a narrow cytoplasmic bridge but a relatively broad
zone of common cytoplasm (Figs. 1.7C and 1.13B ). The
nurse cell separates from the mature oocyte at ovulation.
In Callopora lineata , as the nurse separates, it takes with it
some yolk granules from the cytoplasm of the oocyte
(Fig. 1.6D ). It is unlikely they are formed in the nurse cell as
they are much larger than its usual inclusions.
1.3.5 Matrotrophic Brooding
Extraembryonic nutrition (EEN) or matrotrophy is the direct
parental provisioning of an embryo with nutrients during
incubation. This is one of the most effective modes of parental
care, evolving independently in more than half of all metazoan
phyla, including Porifera, Cnidaria, Platyhelminthes and
Nematoda (both free-living and parasitic), Nemertea,
Annelida, Mollusca, Bryozoa, Kamptozoa, Arthropoda,
Onychophora, Echinodermata, Chordata and some other
groups (see Giese and Pearse 1974 , 1975a , b , 1977 ; Giese
et al. 1979 , 1991 ; Adiyodi and Adiyodi 1989 , 1990 ; Blackburn
2005a ; Wourms et al. 1988 ; Batygina et al. 2006 ; and references therein). The simplest mode of matrotrophy is histotrophy, that is, absorption via embryonic epithelium, whereas
the most complex is placentotrophy, which, according to
Mossman’s ( 1937 , p. 156) widely accepted defi nition of a
placenta, involves “any intimate apposition or fusion of the
fetal organs to the maternal [or paternal] tissues for physiological exchange”. In addition to therian mammals, placentas
are widely documented among squamate reptiles, fi shes
(reviewed in Wourms 1981 ; Wourms et al. 1988 ; Wourms and
Lombardi 1992 ; Blackburn 1992 , 1993 , 1999 , 2005a , b ;
Blackburn et al. 1985 ; Wooding and Burton 2008 ) and invertebrates, being often referred to as placental analogues or
sometimes pseudoplacentas (Turner 1940 ; Hagan 1951 ;
Blackburn 1999 ; Farley 1996 ). Despite the two latter terms
being considered archaic, “placental analogue” still seems
suitable for describing the simplest placentas of some invertebrates. The main reason for this is that close apposition
between the embryo and the nutritive organ or tissue is often
established during the later stages of incubation. Prior to this,
the embryo grows suspended in a brood cavity without any
contact with the maternal wall that provides nutrition, absorbing nutrients from the surrounding fl uid of the incubation
chamber. Thus, there is matrotrophic nutrition, but not placentation in the strict sense during much of the incubation
period (Ostrovsky 2013 ).
In most groups including species with EEN, the majority
of species are either egg-laying or non-matrotrophic livebearing animals. Known exceptions are trematodes
(Platyhelminthes), the arthropod orders Scorpiones,
Pseudoscorpiones and Strepsiptera, and salps and mammals
among chordates. All species in these groups have EEN
(Hagan 1951 ; Weygoldt 1969 ; Francke 1982 ; Godeaux 1990 ;
Lombardi 1998 ; Galaktionov and Dobrovolskij 2003 ;
Blackburn 2005a ). Phylum Bryozoa is another example, in
which all living representatives of the classes Stenolaemata
and Phylactolaemata and many species from the class
Gymnolaemata are known or inferred to be matrotrophic
(Ostrovsky 2009 ; Ostrovsky et al. 2009a ). Moreover, in contrast with the vast majority of matrotrophic animals that are
viviparous, many matrotrophic bryozoans are brooders and
incubate their embryos outside the parental body cavity.
Apart from the Pseudoscorpionida and Salpida, matrotrophic
brooding is generally regarded as rare and is known in several
chordates (ascidians, bony fi shes and amphibians), a handful
of bivalve and gastropod molluscs, and a few crustaceans,
kamptozoans and echinoderms (Mukai et al. 1987 ; Hoese
and Janssen 1989 ; Nielsen 1990 ; Warburg and Rosenberg
1996 ; Lombardi 1998 ; Schwartz and Dimock 2001 ;
Korniushin and Glaubrecht 2003 ; O’Loughlin et al. 2009 ).
1.3.5.1 Historical Overview
Extant species from the viviparous order Cyclostomata (class
Stenolaemata) and the brooding class Phylactolaemata are
all matrotrophic. It has long been known that their embryos
enlarge during incubation and the anatomy of supposed
placental analogues has been described (Harmer 1893 ;
Braem 1897 , 1908 ; Borg 1926 ; Brien 1953 ).
In contrast, EEN was until recently considered to be rare
in gymnolaemates. There are relatively few records in the
historical literature, citing such features as embryonic
enlargement during incubation and hypertrophied epithelial
walls in brood chambers. Although providing evidence for
1 Reproductive Patterns of Gymnolaemate Bryozoa: General Overview and Comparative Analysis