259
brood their embryos, with only four species in four different
families having cyphonautes larvae – Alcyonidium albidum
(Alcyonidiidae),
Farrella
repens
(Triticellidae),
Hypophorella expansa (Hypophorellidae) and Hislopia
malayensis (Hislopiidae) (Ström 1977 ; Zimmer and
Woollacott 1977a ; Wood 2008 ; Nielsen and Worsaae 2010 ).
The reproductive mode and early development of both F .
repens , described by Marcus ( 1926a ), and H . expansa (see
Prouho 1892 ) indicate that their larvae are truly cyphonautes,
but their later stages, although presumably shelled, are
unknown (discussed in Zimmer and Woollacott 1977a ;
Waeschenbach et al. 2012 ). Nevertheless, the presence of the
intertentacular organ in many Alcyonidium species and some
other ctenostomes (see Table 1.9 , reviewed in Ostrovsky and
Porter 2011 ) indicates that planktotrophy is not so rare in this
order. Some ctenostomes also have matrotrophic brooding
(reviewed in Ostrovsky et al. 2008a ; see also Ostrovsky and
Schwaha 2011 ).
The diversity of reproductive patterns in ctenostomes is
an inviting fi eld of study, promising a detailed reconstruction
of the evolutionary stages of sexual reproduction not only
within this order but within the whole phylum. At present,
most descriptions of ctenostome sexual reproduction in the
literature contain only a perfunctory characterization of
oogenesis and often one cannot be sure about the exact
reproductive pattern. Besides, the productivity of the female
gonad throughout the reproductive period has never been
assessed, and the numbers of oocytes in the ovary and the
coelom as well as the numbers of brooded embryos (see
below and Table 3.2 ) refl ect only the state of things at the
moment of study/collection. Therefore, the account that follows may be somewhat incomplete and imprecise, and
should be treated as a fi rst attempt at revealing the evolution
of sexual reproduction in ctenostomes based on the data in
the literature.
Reproductive pattern I in Ctenostomata is similar to that
in Cheilostomata. Numerous (from 10–15 to 60) small
oocytes 25–90 μm in diameter are formed in the ovary. Most
or some of them ripen, ovulate (in groups of 5–15 oocytes),
are fertilized and released. These eggs are oligolecithal and
develop into planktotrophic larvae. Apparently this pattern
was also characteristic of the earliest ctenostomes.
Other reproductive patterns in ctenostomes differ in some
respects from the corresponding patterns of cheilostomes.
Pattern II is characterized by the brooding and production
of lecithotrophic larvae that develop from oocytes containing
more nutrients than oocytes in species with pattern I.
Ctenostomes appear to have several variants of pattern II,
differing in the number and size of female gametes formed in
the ovary and in the number of brooded embryos (see
Table 3.2 ), viz (1) several dozen small oocytes are formed in
the ovary, attaining 65 μm diameter upon maturation; then
they ovulate (up to 60), are released and externally brooded
in groups of 2–4 up to 20, each developing into non-feeding
larva ( Triticella fl ava ); (2) 20–40 small female gametes are
formed in the ovary but apparently only 4–8 of them mature,
being rather large (>100 μm diameter); then they ovulate, are
released and brooded externally, usually one by one
( Paludicella articulata , Potsiella erecta ); (3) from 4 to 10–12
or even 19 oocytes are formed in the ovary; upon maturation
they can be small (50–90 μm), medium-sized (100–200 μm)
or large (>300 μm); further, the eggs ovulate, are released
and brooded in groups of 2–6 (up to 12) ( Alcyonidium
duplex , A . polyoum , A . eightsi , A . hirsutum , A . diaphanum ,
Tanganella muelleri , T . appendiculata , Bulbella abscondita ,
Panolicella nutans ); (4) 1–5 relatively small (80–90 μm) or
very large (up to 370 μm) oocytes are produced in the ovary,
ovulate sequentially, and are brooded in the introvert one by
one ( Bowerbankia imbricata , B . gracilis , B . pustulosa ,
Alcyonidium disciforme , Terebripora comma ). Judging from
the illustrations in the literature, different species of brooding non-matrotrophic ctenostomes have mesolecithal or
macrolecithal oocytes with a size range from small to very
large. The above pattern II variants may be arranged in a
series representing a trend towards a gradual decrease in
number and increase in size of the produced oocytes and the
brooded embryos.
Pattern III is characterized by small eggs, extraembryonic
nutrition and endotrophic larvae. Contrary to cheilostome
matrotrophs with pattern III that produce a small number of
oocytes (usually 1–2 doublets) and brood embryos one by
one, such ctenostomes produce from 2–3 to 100 female gametes, of which 1–10 mature as small oligo- or mesolecithal
oocytes; they ovulate and are brooded one by one or in
groups of 2–5, considerably enlarging during embryogenesis. Ctenostome species that appear to have pattern III, judging from the available descriptions and illustrations, are
Labiostomella gisleni , Sundanella sibogae , Nolela dilatata ,
N . stipata , N . gigantea , Walkeria uva , Bantariella cookae
and Zoobotryon verticillatum .
The ctenostome Flustrellidra hispida supposedly has
reproductive pattern IV. The ovary produces 4–5 gametes
that grow into relatively small macrolecithal oocytes about
100 μm diameter and after ovulation are brooded simultaneously in a brood chamber (Pace 1906 ). Larval enlargement
indicates the presence of extraembryonic nutrition.
Nevertheless, despite the advanced brooding type,
Flustrellidra hispida has a primitive endotrophic pseudocyphonautes larva with chitinous valves and a rudimentary gut.
If we take pattern I as the starting point, the evolution of
sexual reproduction in the order Ctenostomata may be represented as follows:
(1) The transition from pattern I to pattern II was connected with the origin of ctenostomes with primitive brooding in external sacs and numerous small oocytes in the
ovary, which, however, accumulated enough nutrients for the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
brood their embryos, with only four species in four different
families having cyphonautes larvae – Alcyonidium albidum
(Alcyonidiidae),
Farrella
repens
(Triticellidae),
Hypophorella expansa (Hypophorellidae) and Hislopia
malayensis (Hislopiidae) (Ström 1977 ; Zimmer and
Woollacott 1977a ; Wood 2008 ; Nielsen and Worsaae 2010 ).
The reproductive mode and early development of both F .
repens , described by Marcus ( 1926a ), and H . expansa (see
Prouho 1892 ) indicate that their larvae are truly cyphonautes,
but their later stages, although presumably shelled, are
unknown (discussed in Zimmer and Woollacott 1977a ;
Waeschenbach et al. 2012 ). Nevertheless, the presence of the
intertentacular organ in many Alcyonidium species and some
other ctenostomes (see Table 1.9 , reviewed in Ostrovsky and
Porter 2011 ) indicates that planktotrophy is not so rare in this
order. Some ctenostomes also have matrotrophic brooding
(reviewed in Ostrovsky et al. 2008a ; see also Ostrovsky and
Schwaha 2011 ).
The diversity of reproductive patterns in ctenostomes is
an inviting fi eld of study, promising a detailed reconstruction
of the evolutionary stages of sexual reproduction not only
within this order but within the whole phylum. At present,
most descriptions of ctenostome sexual reproduction in the
literature contain only a perfunctory characterization of
oogenesis and often one cannot be sure about the exact
reproductive pattern. Besides, the productivity of the female
gonad throughout the reproductive period has never been
assessed, and the numbers of oocytes in the ovary and the
coelom as well as the numbers of brooded embryos (see
below and Table 3.2 ) refl ect only the state of things at the
moment of study/collection. Therefore, the account that follows may be somewhat incomplete and imprecise, and
should be treated as a fi rst attempt at revealing the evolution
of sexual reproduction in ctenostomes based on the data in
the literature.
Reproductive pattern I in Ctenostomata is similar to that
in Cheilostomata. Numerous (from 10–15 to 60) small
oocytes 25–90 μm in diameter are formed in the ovary. Most
or some of them ripen, ovulate (in groups of 5–15 oocytes),
are fertilized and released. These eggs are oligolecithal and
develop into planktotrophic larvae. Apparently this pattern
was also characteristic of the earliest ctenostomes.
Other reproductive patterns in ctenostomes differ in some
respects from the corresponding patterns of cheilostomes.
Pattern II is characterized by the brooding and production
of lecithotrophic larvae that develop from oocytes containing
more nutrients than oocytes in species with pattern I.
Ctenostomes appear to have several variants of pattern II,
differing in the number and size of female gametes formed in
the ovary and in the number of brooded embryos (see
Table 3.2 ), viz (1) several dozen small oocytes are formed in
the ovary, attaining 65 μm diameter upon maturation; then
they ovulate (up to 60), are released and externally brooded
in groups of 2–4 up to 20, each developing into non-feeding
larva ( Triticella fl ava ); (2) 20–40 small female gametes are
formed in the ovary but apparently only 4–8 of them mature,
being rather large (>100 μm diameter); then they ovulate, are
released and brooded externally, usually one by one
( Paludicella articulata , Potsiella erecta ); (3) from 4 to 10–12
or even 19 oocytes are formed in the ovary; upon maturation
they can be small (50–90 μm), medium-sized (100–200 μm)
or large (>300 μm); further, the eggs ovulate, are released
and brooded in groups of 2–6 (up to 12) ( Alcyonidium
duplex , A . polyoum , A . eightsi , A . hirsutum , A . diaphanum ,
Tanganella muelleri , T . appendiculata , Bulbella abscondita ,
Panolicella nutans ); (4) 1–5 relatively small (80–90 μm) or
very large (up to 370 μm) oocytes are produced in the ovary,
ovulate sequentially, and are brooded in the introvert one by
one ( Bowerbankia imbricata , B . gracilis , B . pustulosa ,
Alcyonidium disciforme , Terebripora comma ). Judging from
the illustrations in the literature, different species of brooding non-matrotrophic ctenostomes have mesolecithal or
macrolecithal oocytes with a size range from small to very
large. The above pattern II variants may be arranged in a
series representing a trend towards a gradual decrease in
number and increase in size of the produced oocytes and the
brooded embryos.
Pattern III is characterized by small eggs, extraembryonic
nutrition and endotrophic larvae. Contrary to cheilostome
matrotrophs with pattern III that produce a small number of
oocytes (usually 1–2 doublets) and brood embryos one by
one, such ctenostomes produce from 2–3 to 100 female gametes, of which 1–10 mature as small oligo- or mesolecithal
oocytes; they ovulate and are brooded one by one or in
groups of 2–5, considerably enlarging during embryogenesis. Ctenostome species that appear to have pattern III, judging from the available descriptions and illustrations, are
Labiostomella gisleni , Sundanella sibogae , Nolela dilatata ,
N . stipata , N . gigantea , Walkeria uva , Bantariella cookae
and Zoobotryon verticillatum .
The ctenostome Flustrellidra hispida supposedly has
reproductive pattern IV. The ovary produces 4–5 gametes
that grow into relatively small macrolecithal oocytes about
100 μm diameter and after ovulation are brooded simultaneously in a brood chamber (Pace 1906 ). Larval enlargement
indicates the presence of extraembryonic nutrition.
Nevertheless, despite the advanced brooding type,
Flustrellidra hispida has a primitive endotrophic pseudocyphonautes larva with chitinous valves and a rudimentary gut.
If we take pattern I as the starting point, the evolution of
sexual reproduction in the order Ctenostomata may be represented as follows:
(1) The transition from pattern I to pattern II was connected with the origin of ctenostomes with primitive brooding in external sacs and numerous small oocytes in the
ovary, which, however, accumulated enough nutrients for the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata