Ophelia

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Ophelia
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Entoproct life-cycles and the entoproct/ectoproct

relationship
a
Claus Nielsen
a
Marine Biological Laboratory, DK-3000, Heisingør, Denmark
To cite this article: Claus Nielsen (1971): Entoproct life-cycles and the entoproct/ectoproct relationship, Ophelia, 9:2,
209-341
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OPHELIA, 9: 209-341 (December 1971)
ENTOPROCT LIFE-CYCLES
AND THE ENTOPROCTjECTOPROCT RELATIONSHIP
CLAUS NIELSEN
Marine Biological Laboratory, DK-3000 Heisinger, Denmark
CONTENTS
Downloaded by [University of Arizona] at 21:43 29 April 2013
Abstract . . 210 Survey of entoproct life-cycles 271

Introduction _ . 210 Embryology 271
Materials and methods . 211 Budding 276
Entoproct embryology and larval
metamorphosis . 212 Survey of ectoproct life-cycles 277
Fam. Loxosomatidae .. _ . 212 Eurystomata _. . . . . . . . . .. 278
Loxosomella atkinsae . _ . 212 Embryology _. . . . . . . . . .. 278
crassicauda . 214 Budding _ 296
elegans . _ . 215 Cyclostomata _. . . . . . . . . .. 297
fauveli . 216 Embryology 297
harmeri 217 Budding. . . . . . . . . . 299
leptoclini . 226 Phyiactolaemata 300
murmanica . 229 Embryology . . . . . . . . . . . . . . . . . . . .. 300
neapolitana . 229 Budding _ 303
obesa .. _ . 230 Discussion _. . . . . . . . . .. 304
pes _ . 230
phascolosomata . 230 Phylogenetic considerations _ 306
polita .. _ . 230 The origin of the Entoprocta 306
scaura , 233 The origin of the Ectoprocta 309
tethyae . 234 Embryology............. 315
varians . 234 Larvae 315
vivipara . _ . 234 Settling and metamorphosis. . . . . . .. 316
Loxosoma davenporti _ . 237 Body wall _. . . . . . . . . .. 317
jaegersteni . 237 Body cavity _. . . . . . . . . .. 317
okudai _ . 237 Muscles 318
pectinaricola . 238 Ciliation and feeding mechanisms .. 3\9
rhodinicola _ . 241 Alimentary canal _ 321
Fam. Pedicellinidae. . . . . 241 Nephridia. . . . . . . . . . . . . . . . . . . . . .. 322
Pedicellina cernua _ . 242 Nervous system ' . . . .. 323
nutans _ . 250 Reproductive organs 325
Sangavella vineta . 254 Spermatozoa. . . . . . . . . . . . . . . . . . . .. 326
Barentsia benedeni _ . 254 Budding and regeneration. . . . . . . .. 329
discreta _ , 254 Resting bodies (hibernaculae) 330
gracilis . 256 Conclusion. . . . . . . . . . . . . . . . . . . . . . . . .. 332
kovalevskii _ . 267 References 332
laxa . 267
Urnateila gracilis _ . 269
14
210 CLAUS NIELSEN
ABSTRACT
The larvae of several entoproct species and their metamorphosis or budding are described and the
literature on entoproct development reviewed. Most species probably have spiral cleavage; some
larvae, such as those of Loxosomella elegans and Loxosoma pectinaricola, are rather schematic
trochophores, whereas most other larvae are highly characteristic, having a frontal organ and a
large ciliated foot.
The larvae of species such as Loxosomella harmeri undergo a metamorphosis; they attach by
means of the contracted frontal organ and the alimentary canal rotates 90 0 in the median plane
with the mouth first. Other loxosomatids, such as Loxosomella leptoclini and L. vivipara, have no
metamorphosis; buds develop from the episphere of their larvae and the larvae die after the
liberatio~ of the buds. Loxosomella polita, in which the metamorphosed larvae never grow to
a normal size or develop the differentiated "foot" characteristic of the adult specimens which
have originated from buds, represents an intermediate type.

The larvae of the pedicellinids attach with the area above the contracted prototroch, becom-
ing glued to the substratum by the secretion of the three pairs of foot glands. Their alimentary
0
canals undergo a 180 rotation.
The literature on life-cycles of the three ectoproct groups Eurystomata, Cyclostomata and
Phylactolaemata is reviewed. Although several problems are in need of further investigation, it
seems clear that the three groups have comparable life-cycles and that the eurystomes represent
the least specialized type.
The origin of the Entoprocta is discussed, and it is concluded that they are related to other
groups having trochophore larvae. The entoprocts having larvae which settle with the frontal
organ are considered primitive and may be derived from a trochophore-like ancestor. The other
types of development are regarded as caenogenetic specializations.
The theories about the origin of the Ectoprocta are discussed. The derivation from a phoronid-
like ancestor is rejected on the basis of a comparison of metamorphoses and budding patterns
in the two groups. It is suggested that the ectoprocts have developed from entoproct-like ances-
tors which have had a metamorphosis similar to that of the pedicellinids and internal budding
like the adults of Loxosomella bocki and the larvae of Loxosomella vivipara and Loxosoma jaeger-
steni. Detailed similarities in the metamorphosis of the two types support this theory, as do the
similarities in the budding and the formation of hibernaculae. The body cavity of the Ectoprocta
is a "fluid skeleton" which probably has developed in connection with the evolution of a
retractable lophophore. Nothing indicates that a "coelom" has been present in the entoprocts.
The most important differences between the ento- and the ectoprocts seem to lie in the cleavage
patterns and the feeding mechanisms, but these differences do not seem to be sufficient for
separating the two groups entirely.
The final conclusion is that the Entoprocta and the Ectoprocta together must represent a
separate phylum, the Bryozoa.
INTRODUCTION
The relationship between the Entoprocta and the Ectoprocta has been a matter of
discussion for almost a hundred years. The early authors simply treated the species
of Pedicellina and Loxosoma together with the ectoprocts under the heading
Bryozoa (or Polyzoa) (van Beneden, 1845; Dalyell, 1848; Hincks, 1851; Kefer-
stein, 1862; Claparede, 1863).
Nitsche (1869) pointed out some of the principal differences between the two
ENTOPROCT LI FE-CYCLES 211
groups and introduced the names Entoprocta and Ectoprocta. Most succeeding
authors have emphasized the differences between the two groups and treated them
as representing separate phyla: Bryozoa (Ectoprocta) and Entoprocta (Kampto-
zoa) (Hatschek, 1891; MacBride, 1914; Korschelt, 1936; Kaestner, 1954, 1963;
Hyman, 1951, 1959; Hadzi, 1958; Brien, 1959, 1960, 1970), but some authors stick
to the old idea of uniting the two groups under the name Bryozoa (Ehlers, 1890;
Harmer, 1915, 1930; Barrois, 1925; Marcus, 1940, 1958; Pflugfelder, 1970).
The previous phylogenetic considerations have been based on knowledge of
the anatomy of the adults and of the larval types and metamorphoses of Pedicel-
lina and several ectoproct species. Recent studies on entoproct larvae have, how-
ever, demonstrated a considerable variation of the life-cycles within the Entoprocta
(Jagersten, 1964; Nielsen, 1966a, 1967a, b), and it was felt that a study of the life-
cycles of a number of entoproct species might give a clue to the understanding of
the relationships between the two groups.
MATERIALS AND METHODS
Samples of various entoproct species have been collected around Helsinger and
during visits to other marine biological laboratories. Specimens carrying large
embryos in the atrium have been isolated in small Boveri dishes, and free-swim-
ming larvae could usually be observed the next day. The specimens of Loxosomella
harmeri have been fed a suspension of Isochrysis and Monochrysis, but the other
species have not been fed. The larvae of L. harmeri were offered loose elytra of the
normal host, the polychaete Gattyana cirrosa, to settle on, and pieces of hydroids
and algae were given to the larvae of Pedicellina and Barentsia.
Live larvae and the various stages of their budding or metamorphosis have
been studied in both transmitted and incident light. All drawings have been made
with a camera lucida. The specimens to be drawn have usually been narcotized
with cocain and killed with one or two drops of formalin. Larvae treated in this
way resemble creeping larvae, but their foot is not fully expanded.
Specimens to be sectioned have been narcotized with cocain, fixed in Bouin's
fluid in sea water and transferred to 70 % alcohol. It has been found that a mod-
erately intense staining with Mayer's haem alum not only makes it easy to orient
the specimens but also makes the nuclei stand out more clearly in the photomicro-
graphs of the sections. The specimens were embedded in epon and sectioned with
a glass knife mounted on a Minot-microtome (Reichert). All species were serially
sectioned at 2 fJ. except Loxosoma pectinaricola, which was sectioned at 3 fJ.. The
sections were stretched individually on drops of acetone. Eukitt was used as
mountant. All photographs have been taken with phase-contrast (Zeiss: Planapo
40 x, n. a. 1.0, or Planapo 100 X, n. a. 1.3).
Important parts of my material have been collected during stays at Havbiolo-
14'
212 CLAUS NIELSEN
gisk Laboratorium, Frederikshavn, Denmark; Kristinebergs zoologiska Station,

Fiskebackskil, Sweden; and Stazione Zoologica, Naples, Italy; my sincere thanks
are due to these institutions for hospitality and good working conditions and to the
Nordic Council for Marine Biology and the Danish committee for collaboration
with the Stazione Zoologica, Naples, for financial support.
Thanks are also due to the Danish Natural Science Research Council for a
grant covering the microscopical equipment and to the Zoological Laboratory of
the Royal Veterinary University for providing the glass knives.
Finally I wish to thank Miss Harriet H. Hansen for her very skillful and en-
thusiastic work with the serial sectioning, and Mr. Kai Olsen for making most
of the drawings after my sketches.
ENTOPROCT EMBRYOLOGY AND

LARVAL METAMORPHOSIS
The Entoprocta are usually divided into three families: Loxosomatidae, Urnatel-
lidae and Pedicellinidae. It appears, however, that the Urnatellidae, which only
comprises one genus with two or three species, is very close to the genus Barentsia
within the Pedicellinidae.
Fam. LOXOSOMA TIDAE

This family comprises solitary species which lack the "star" cell complex at the
transition between the calyx and stalk. Four genera have been described of which
two, viz. Loxomespilon and Loxostemma, comprise one species each. A new in-
vestigation of Loxomespilon perezi (Emschermann, 1971) has shown that this
species is closely related to the subgenus Loxomitra within Loxosomella. The po-
sition of Loxostemma is still uncertain.
Loxosomella atkinsae Bobin & Prenant, 1953

NEW OBSERVATIONS: A specimen of the sipunculid Phascolion strombi (Montagu)
with a small growth of this species was collected from a mixed bottom, depth 30-35
metres, at Gaso Ranna (near the Kristinebergs zoologiska Station, on the Swedish
west coast), 18 August 1970. A few individuals carried up to six embryos in the
atrium, and larvae were liberated after one day.
The larva (Fig. 1) resembles that of L. elegans very closely. It is about 70 fl.
high when swimming and has an oval prototroch with a width of about 80 fl.
(without the cilia); the row of prototroch cells curves inwards at the posterior end
where the large syncilia are lacking. A ring of small cilia lies above the large syn-
cilia. The apical organ is well developed with a tuft of long cilia; a frontal organ
has not been observed. The hyposphere is almost totally ciliated and there is no
ENTOPROCT LIFE-CYCLES 213
8
100 fJ
o E
FIG. 1. Loxosomella atkinsae. A-C, a swimming larva in apical, frontal and lateral views; D-E,
a contracted larva in lateral and frontal views.
trace of a foot. The larva is rather transparent and the digestive tract can easily
be seen through the body wall. The only feature which makes it possible to dis-
tinguish this larva from that of L. elegans is the number of large vacuolated cells
occurring at the sides of the base of the apical organ and further down on the epi-
sphere, partly hidden by the prototroch. The larva of L. atkinsae has two pairs of
these cells near the apical organ and two pairs near the prototroch, while the larva
of L. elegans has one pair near the apical organ and three pairs near the prototroch.
These vacuolated cells are especially easily seen in the contracted larva.
The further development has not been followed.
This species often occurs together with L. murmanica, which has a larva of the
usual swimming-creeping type, with a well-developed foot. The larval type is thus
a very good distinguishing character between these two species.
214 CLAUS NIELSEN
o E F
FIG. 2. Loxosomella crassicauda. A-C, a swimming larva in lateral, frontal and apical views;
D-E, a specimen about two days after settling, in frontal and posterior views; F, the same speci-
men in lateral view, slightly pressed under the cover glass.
Loxosomella crassicauda (Salensky, 1877)

NEW OBSER VA nONS: A number of specimens were found on a stone with dead
Lithothamnion dredged from a stony bottom, depth about 45 metres, near La
Gaiola (Bay of Naples), 16 May 1967. The adult specimens agreed well with the
descriptions given by Salensky (1877) and Atkins (1932a) except that the gland-
ular cells behind the upper part of the lophophore were not observed.
A few larvae were obtained (Fig. 2 A-C). When swimming they were about
150 fL long and about as wide. The prominent frontal organ showed a pair of eyes.
The episphere had a symmetrical pattern oflarge cells filled with a granular material.
One of the larvae had settled after about one day. It had attached to the sub-
stratum by means of the contracted frontal organ and had closed the atrium com-
pletely. The larva was fixed two days after it settled (Fig. 2D-F), and although
the atrium had not yet reopened, the alimentary canal had already acquired the
orientation seen in the adult. The degenerating apical and frontal organs were
still visible; the pigment of the eyes was lying close to the frontal side of the
oesophagus.
Loxosomella elegans Nielsen, 1964

LITERATURE: The newly released larva was figured and briefly described in an ear-
lier paper (Nielsen, 1967b). It is small and has an oval prototroch with a width of
about 90 fL (without the cilia). It has a large apical organ, but lacks a frontal organ.
There is no trace of a foot.
NEW OBSERVA nONS: Sections have been made oflarvae released from a number
of adults found in tubes of the maldanid polychaete Praxillella praetermissa
(Malmgren); the material was dredged from a mixed bottom off Odinshej (north-
ern part of the 0resund), depth 25-28 metres, October 1968.
The drawings of the larva given here (Fig. 3) are slightly modified from those
given in my earlier description; sectioning has revealed a ring of small cilia above
the large syncilia of the prototroch and a pair of areas devoid of cilia on the sides
of the anus.
The sections furthermore show a small frontal ganglion (Fig. 5), but there is
no frontal organ. A pair of nerves connect the apical organ with the frontal ganglion
and proceed to the latero-frontal part of the ring of prototroch cells. A pair of
muscles follows these nerves, but inserts on the sides of the oesophagus near the
mouth; an unpaired muscle originates at the posterior side of the apical organ and
inserts on the intestine (Fig. 4); these muscles are probably the retractors of the
FIG. 3. Loxosomella elegans. A swimming larva in frontal and lateral views. Slightly modified
from Nielsen (1967 b).
216 CLAUS NIELSEN
FIG. 4. Loxosomella elegans. An almost median section of an expanded larva.
hyposphere. A number of small muscles run between the lateral parts of the epi-
sphere and the hyposphere. The gut shows the usual configuration (Fig. 4); proto-
nephridia have not been observed.
The following development is still unknown.
Loxosomella fauveli Bobin & Prenant, 1953

LITERATURE: Barrois (1877, as Loxosoma singulare) described the development and
the larva of this species on the basis of whole mounts. The early stages of the de-
frontal. gangli~n
FIG. 5. Loxosomella elegans. A transverse section of an expanded larva, showing the ganglion.
50 fl
atrial groove
FIG. 6. Loxosomella elegans. A transverse section of an expanded larva, showing the apical organ
and the stomach.
velopment are rare and difficult to handle, and this may be the reason why his
description and drawing ofthe eight-cell stage (op. cit., pl. 1, fig. 1) does not show
the spiral cleavage pattern characteristic of all other entoprocts investigated so far.
The following stage shows a ring of large prototroch cells at the periphery of
a somewhat flattened embryo. The formation of the alimentary canal and the apical
and frontal organs was apparently difficult to observe in detail because of the opac-
ity of the embryos. The whole gut was said to be formed from an invagination of
the central part of the hyposphere. Cilia first develop on the prototroch cells and
later on also on the apical and frontal organs, and a pair of red eyes develops in
the latter. The foot develops as a thickening inside the curve of the gut, and a trans-
verse slit comes to separate the anterior part of the foot, with the large cirri, from
the posterior part, on which the anus opens.
The fully grown larva (see Fig. 62) is of the same type as that of L. harmeri. It
was observed to creep on the foot and sometimes to attach by means of the
apical organ.
Loxosomella harmeri (Schultz, 1895)

LITERATURE: Nielsen (1967a) mentioned that the metamorphosis of the larva of
this species takes place in the same manner as that of L. murmanica.
NEW OBSERVATIONS: This species is very common on a mixed bottom with shells,
depth 25-30 metres, off Odinshej (northern part of the 0resund). The adults occur
on the upper side of the elytra of the polynoid polychaete Gattyana cirrosa (Pal-
las), which is found in the tubes of the terebellid polychaete Amphitrite cirrata
218 CLAUS NIELSEN
A
FIG. 7. Loxosomella harmeri,

A narcotized larva seen from
the left side, from below and
from above.
FIG. 8. Loxosomella harmeri.

A newly settled larva which
has not yet closed the atrium
completely, seen from below and
from the left side.
A B c
D E F
FIG.9. Loxosomella harmeri. A-C, a rather newly settled specimen in frontal, lateral and posterior
views; D-F, a specimen which has recently completed metamorphosis, in frontal, lateral and
posterior views, note the eye pigment in the oesophagus.
220 CLAUS NIELSEN
stomach apical organ glandular cells above

frontal organ
organ
oesophagus
rectum foot "sale" foot knob syncilium of the foot knob
FIG. 10. Loxosomella harmeri. A median section of an expanded larva.
O. F. Muller. The material treated below was collected in September-December

1966-70.
The newly liberated larvae (Fig. 7) swim rapidly through the water and have an
almost circular prototroch; they keep the foot halfway retracted so that only the
FIG. 11. Loxosomella harmeri. Section no. 6 of FIG. 12. Loxosomella harmeri. Section no. 10
a series of transverse sections of an expanded of a series of transverse sections of an expan-
larva showing the anterior part of the frontal ded larva showing the eyes; some of the cilia
organ surrounded by the glandular cells. of the prototroch have been omitted.
ENTOP ROCT LIFE-CYCLES 221
100 IJ
p,oto~,
oesophagus
atrial groove
FIG. 13. Loxosomella harmeri. Section no. 21 of a series of transverse sections of an expanded
larva, just behind the mouth.
10011
peri pedal groove foot "sole" prototroch
larva, showing the apical organ.
larva, showing one of the lateral sense organs.
222 CLAUS NIELSEN
apical organ
frontal organ
foot knob
FIG. 16. Loxosomella harmeri. A median section of a contracted larva.
foot knob and the posterior part of the foot protrude below the prototroch. When
the larvae touch a substratum or the water film they stretch the foot out and start
to creep; in this state the prototroch is oval, almost one and a half times as long as
wide. The frontal organ is protruded and now and then it becomes pressed against
the substratum. The largest larva observed had a total length of about 230 fl.
when creeping.
Some larvae have a dense cover of whitish "detritus" particles on the episphere,
but other larvae lack these particles completely.
The anatomy is illustrated through one median and five transverse sections
(Figs 10-15). The apical organ is covered by a thick transparent cuticle through
which a number of cilia protrude. There is a ring oflarger syncilia near the periph-
ery of the organ. The frontal organ has a pair of circular ciliated areas with a few
large syncilia and a pair of eyes, each with a reddish-brown pigment cup and an
almost spherical lens at the lateral side. Around the frontal organ is found a ring
of cells which are probably glandular as they contain a number of refractive drop-
lets (Figs 11, 12). In the creeping larva the episphere shows a pair of deep longi-
tudinal infoldings. A little behind the middle of the lateral ridge thus formed
occurs a small sensory organ consisting of a small pit with a tuft of cilia (Fig. 15).
A number of large vacuolated cells form a symmetrical pattern on the episphere.
The nerves and muscles have not been studied.
The prototroch consists of a row of large syncilia protruding from a circle of
large cells. A row of small cilia is found on a ring of cells just above these large
FIG. 17. Loxosomella harmeri. A median section of a rather newly settled larva.
cells. The atrial groove is shallow and provided with a rather sparse cover of cilia.
The peripedal groove is lined by an epithelium which especially in the posterior
part consists of cells with large nuclei (Fig. 15). The foot is ciliated on the sale and
on the whole foot knob. Six large synci1ia form a transverse rowan the anterior
side of the foot knob. A curved row of peculiar epithelial organs occurs in the
same region; these organs consist of an ovoid part filled with a granular mass
(Fig. 13) and a long "spout" which protrudes between the cilia of the foot knob.
Similar organs occur in the posterior part of the foot. There are no large glands
associated with the foot. The digestive tract shows the usual four regions: oeso-
phagus, stomach, intestine, rectum. The anus is situated on the upper side of the
posterior part of the foot.
When the larva has selected a suitable spot for settling it attaches to the sub-
stratum by means of the contracted frontal organ. It is probably the secretion from
the ring of cells around the frontal organ which glues the larva to the substratum.
The hyposphere retracts and the ring of cells above the upper ciliary ring of the
prototroch constricts and encloses the atrium completely (Figs 8, 17). The apical
224 CLAUS NIELSEN
FIG. 18. Loxosomella har meri . A median section of a specimen which has carried' through most
of the metamorphosis.
organ retracts. The posterior part of the foot bends forward along the median part
of the "sole" and the peripedal rims of the two sides approach and almost enclose
the whole foot in a separate cavity. The ciliated cells of the foot separate and start
degenerating; during the following stages of the development they can be found
in the lateral parts of the primary body cavity where they can be recognized by a
large vacuole containing the cilia. The edges of the foot finally meet completely
and form the epithelium of the bottom of the atrium. There seems to be some in-
dividual variation in the timing of the processes just mentioned, but the overall
pattern is constant.
The alimentary canal slowly rotates about 90 in the median plane, with
0
the mouth first. The ganglion forms as a small laterally elongated thickening of the
epithelium of the bottom of the atrium, and is thus formed quite independently of
FIG. 19. Loxosomella harmeri. An almost median section of a specimen which has nearly com-
pleted the metamorphosis; the atrium is still closed by the cuticle.
the nervous system of the larva. The ciliated cells enclosed in the atrium degenerate
and some of them become digested in the gut. The contracted frontal organ persists
as an elongated "gland" in the basal part of the stalk. The pigment of the eyes be-
comes incorporated in some of the cells of the oesophagus. The tentacles develop
as thickenings of the epithelium of the frontal side of the atrium. The cuticle
covers the atrium during this development (Fig. 19) and does not burst before
the first three pairs of tentacles have developed a ciliation (Fig. 9D-F).
During a period the individuals originating from settled larvae can be distin-
guished from the newly settled buds by the presence of the pigment of the eyes
in the frontal part of the oesophagus (Fig. 9 D-E).
15
226 CLAUS NIELSEN
Loxosomella leptoclini (Harmer, 1885)

LITERATURE: In the original description of the species Harmer (1885) gave a rather
detailed description of its embryology. The development takes place in a pair of
brood pouches formed from the lateral parts of the atrium. The egg and the early
stages are small but at a stage when the digestive tract has been formed the embryo
starts to grow rapidly, probably nourished by the high columnar epithelium of the
brood pouch, which is in intimate contact with the episphere of the larva. The
cleavage is total and apparently equal, but no special pattern is mentioned. Pole
cells were not observed. A coeloblastula is soon formed, and the archenteron is
formed through invagination. A pair of mesoderm cells can soon be distinguished
lying close to the blastopore, which closes. The origin of the two mesoderm cells
is difficult to make out, but they are said to give rise to a pair of forward-growing
lateral bands, from which most of the mesoderm of the larva originates. A funnel-
shaped invagination in front of the closed blastopore forms the stomodaeum, and
the rectum is believed to originate as a proctodaeum in the region of the closed
blastopore. The frontal and apical organs are formed as thickenings of the epi-
thelium. The frontal organ is a two-lobed invagination which becomes solid and
which in the older embryos is dumbbell shaped and shows a median fibrillar region
and a pair of eyes, each with a reddish-brown pigment cup and a conspicuous
lens; its surface develops a pair of ciliated depressions in the adult larva. Between
mouth and anus develops a pair of cavities; these soon fuse in the mid-line and
form the vestibule; a foot is not mentioned. The prototroch develops from a
ring of cells with large nuclei. The mouth becomes transversely extended and an
atrial groove runs from the sides of the mouth along the lower side of the proto-
troch. The frontal organ was correctly interpreted as a ganglion, but the apical
organ was called a sucker and was believed to be homologous with the foot gland
of the adults. The free-swimming larvae were photopositive. They settled after a
few hours, but did not become permanently attached to the substratum.
Some larvae were kept alive for a few days and they produced a pair of lateral
buds above the prototroch. These buds resembled the buds of the adult loxosoma-
tids, but the larvae died before the buds had become ready to detach. Sections
showed that the larval gut transforms into a solid mass of cells when the budding
begins. It was believed that the epithelia of the lophophore and the atrium form
from the ectoderm in the bud while the gut should originate from the cells of the
larval gut. It was presumed that the larva would die after having liberated the two
buds.
The following year Harmer (1886) described the metamorphosis of Pedicellina
cernua, and in view of these observations he proposed that the degeneration of the
larval gut described above was abnormal.
A
FIG. 20. Loxosomella leptoc/ini. A, calyx of an adult specimen with three embryos in the atrium,
posterior view; B-C, a newly settled larva in normal resting position and creeping slowly after
a strong irritation; D-E, two larvae, each carrying a pair of large buds, specimens fixed imme-
diately after capture.
NEW OBSERVATIONS: A rich material was obtained from a stony bottom, depth
about 40 metres, near La Gaiola (Bay of Naples), May-June 1967. The specimens
occurred in abundance on somewhat incrusted, orange and brownish-grey colo-
nies of the colonial ascidian Didemnum maculosum (Milne Edwards); they were
never found on the more soft, grey or pink colonies.
A number of the individuals had a large and one or two small embryos in the
atrium (Fig. 20A). The large larvae were released after a few days and swam
rapidly through the water (Fig. 21 A-C); they were clearly photopositive. The
swimming larva has a prototroch which is about 120 fL wide and 105 fL long
(without the cilia). The apical and frontal organs are well developed and the latter
has a pair of reddish-brown eyes. There is a large foot which carries six stout
syncilia on the foot knob.
After less than one day the larvae attached to a substratum by means of the
somewhat contracted foot, with the prototroch retracted and pressed against the
sides of the foot. The apical and frontal organs were kept retracted. During the
first days of the following development the larvae reacted to being touched or to
IS·
228 CLAUS NIELSEN
100 fJ
FIG. 21. Loxosomella leptoclini. A-C, a narcotized larva seen from below, from above and from
the left side; D, a newly settled larva with two small buds, apical view; E, a larva carrying one
large bud, about two days after the settling; F, a degenerating larva carrying one bud, which is
almost ready for being liberated, about four days after the settling.
other stimuli by pressing the body against the substratum, and if the irritation
was strong enough they even started to creep slowly (Fig. 20 B-C).
About one day after the settling a pair of lateral, hemispherical buds had
developed a little above the contracted prototroch (Fig. 21 D). The buds seemed to
develop in the same way as those of the adults. In the specimens kept in the
dishes usually only one bud developed to full size (Fig. 21 E-F), and this develop-
ment lasted about four days. Larvae with two buds of equal size (Fig. 20, D-E)
were, however, obtained from a Didemnum which had been fixed immediately
after capture, and I believe that both buds normally develop to full size. The lar-
vae slowly degenerate during the budding, and they probably die after having
liberated the buds.
Loxosomella murmanica (Nil us, 1909)

LITERATURE: The fully grown larva and its metamorphosis were described in an
earlier paper (Nielsen, 1967a) and Franzen (1970b) gave a fine drawing of the
larva. The larva resembles that of L. harmeri but lacks the pigmented eyes. It
creeps and swims for a few days and then attaches to the substratum by means of
the contracted frontal organ. The prototroch contracts and the ring of cells just
above the ciliated cells constricts; the whole hyposphere and the prototroch thus
become enclosed in a cavity. The foot and the apical organ degenerate and the
0
alimentary canal rotates about 90 After about one week the atrium reopens,
•
already with small ciliated tentacle buds at its periphery.
NEW OBSERVATIONS: The larva pictured in Fig. 22 was liberated from a small
growth of adults found in a tube of the pectinariid polychaete Amphictene auri-
coma (0. F. Miiller) dredged from a mixed bottom off Odinshej (northern part of
the 0resund), depth 27 metres, 8 May 1967.
Loxosomella neapolitana (Kowalewsky, 1866)

LITERATURE: In the original description Kowalewsky (1866) gave a short descrip-
tion of some developmental stages and of the larva. The frontal organ, which
100 IJ
FIG. 22. Loxosomella
murmanica.
A creeping larva seen from
the left side.
230 CLAUS NIELSEN
was interpreted as the mouth of the larva, is large and has a pair of ciliated areas.
The prototroch is, almost circular and there is a well-developed foot.
Loxosomella obesa (Atkins, 1932)

LITERATURE: Atkins (1932 a) gave a description of the fully grown larva (see Fig.
62) which is rather similar to the larva of L. harmeri. It has a pair of reddish-brown
eyes. Staining revealed some large mucus glands "on the floor of the vestibule".
Some larvae survived for up to seven days but none of them settled.
Loxosomella pes (Schmidt, 1878)

LITERATURE: Schmidt (1876, as Loxosoma singulare) gave two drawings of young
embryos and one of a larva. It is not clear if the larva is seen from above or from
below, but the three pairs of groups of spherical bodies (7) may correspond to the
"bumps" described by Jagersten (1964) from the "type A" larva.
Loxosomella phascolosomata (Vof?;t, 1876)

LITERATURE: In the original description of the species Vogt (1876) gives some
information on the development of the embryos and the morphology of the larva.
The cleavage of the eggs was not studied in detail, but a gastrula stage is mentioned;
how the gastrulation took place could not be observed, but it was thought to be
through epiboly. From the drawings of the later stages (op. cit., pl. 13) it is quite
clear that the stomach, the intestine and the rectum with the anus were taken for
the archenteron with the blastopore. The older stages of the embryos and the lib-
erated larva have a well-developed circular prototroch, a paired ciliated retractile
frontal organ ("spectacle organ") with a pair of red eyes, and a ciliated retractile
apical organ ("tail"). The posterior part of the foot with small cilia protrudes
below the prototroch; it was taken for a mouth cone; the mouth and the oesopha-
gus were overlooked.
Cori (1929) gave two drawings of a larva (see Fig. 62), showing an elongated
prototroch and prominent apical and frontal organs; the latter has a pair of cil-
iated areas and a pair of eyes. The hyposphere has an atrial groove and a well-
developed foot with eight large syncilia on the foot knob.
Loxosomella polita Nielsen, 1964

NEW OBSERVATIONS: Abundant material of this species was found in tubes of the
maldanid polychaete Petaloproctus tenuis borealis Arwidsson, obtained from a
mixed bottom with shells off Odinshej (northern part of the 0resund), depth
25-28 metres, September-December 1966-67.
100 IJ
FIG. 23. Loxosomella polita. A narcotized larva seen from above, from below and from the
left side.
The larva (Fig. 23) resembles that of L harmeri. When narcotized it has an
oval prototroch with a length of about 130 fL and a width of about 100 fL (without
the cilia). The apical organ is rather small, but the frontal organ is well developed
with a pair of reddish eyes. The episphere usually carries a sparse cover of "detri-
tus" particles. The hyposphere shows the usual ciliation and a foot which carries
six syncilia on the foot knob.
232 CLAUS NIELSEN
c
FIG. 24. Loxosomella polita. A-C, a newly settled larva with a small bud, seen from below, from
above and from the right side; D-E, a rather newly settled specimen which has developed a large
bud, seen from above and below; F, sketch of an almost median section of the specimen shown
in D-E. Both specimens from tubes of Petaloproctus.
100 fJ
FIG. 25. Loxosomella seaura. A narcotized larva seen from the right side and from below.
The metamorphosis has not been followed, but some newly settled larvae have
been found in the tubes of Petaloproctus. They were recognized by the pigment
cups of the eyes. The larvae had settled with the area around the contracted frontal
organ and had constricted the prototroch. A small bud was observed at one side
of the youngest specimen (Fig. 24A-C). The somewhat older specimens had larger
buds (Fig. 24D-F) and had almost completed their metamorphosis. They do,
however, not develop the differentiated "foot" at the base of the stalk character-
istic of all the large specimens. I have observed several small adults without a
foot and with only two or four quite short tentacles. I believe that the specimens
without a foot are metamorphosed larvae, and that these specimens usually degen-
erate after having given off a bud. They may carry through most stages of a
normal metamorphosis, as that observed in L. harmeri, but they do not grow to
full size or develop the normal number of tentacles. All specimens with a foot
must have originated as buds.
Loxosomella scaura Nielsen, 1964

NEW OBSERVATIONS: Some larvae were obtained from a population on the neph-
tyid polychaete Nephtys paradoxa Malrn collected from a muddy bottom off Ly-
sekil (Swedish west coast), depth about 50 metres, 9 September 1969.
The larva (Fig. 25) resembles that of L. harmeri. When swimming it has an
oval prototroch with a length of about 150 fL and a width of about 125 fL (without
the cilia); the creeping larva is somewhat more elongated. The eyes have pink
pigment cups.
234 CLAUS NIELSEN
Loxosomella tethyae (Salensky, 1877)

LITERATURE: Harmer (1885) described a few stages of the embryology and gave
some notes on the morphology of the fully grown larva. The cleavage of the egg
is equal and the gastrula forms through invagination. A pair of mesoderm cells is
found in the narrow blastocoele of the young gastrula. The following development
resembles that of L. leptoclini, but the embryos are attached to the embryophore
in the normal way.
The larva, which is devoid of eyes, is said to resemble that of L. pes, which was
very summarily described and figured by Schmidt (1876).
Loxosomella varians Nielsen, 1964

NEW OBSERVATIONS: A few larvae were obtained from some populations growing
on polychaetes of the genus Nephtys dredged from mixed bottoms off Odinshej
(northern part of the 0resund), depth 25-30 metres, November 1966-67.
The larva (Fig. 26) is small and rather characteristic. It is devoid of eyes and
has a slightly oval prototroch which is about 85 fL long and about 70 fL wide (with-
out the cilia). There is a normal apical organ and a large frontal organ which is
usually strongly protruded and whose ciliated area forms one slightly transversely
elongated knob. A ring of cells containing small refractive droplets encircles this
organ. The episphere is in many cases covered with a dense layer of very small par-
ticles. The hyposphere has the same morphology as that of the larva of L. harmeri.
The metamorphosis has not been followed, but the presence of the glandular
cells around the frontal organ suggests that the larva settles like that of L. harmeri.
Loxosomella vivipara Nielsen, 1966

LITERATURE: The very aberrant development of this species has been described in
an earlier paper (Nielsen, 1966a). The very small egg cleaves equally and the eight-
cell stage shows the characteristic spiral pattern (Fig. 27A). The following stages
are, however, more irregular and the spiral pattern is completely lost. At a stage
of 62 cells four apical cells are situated in a small invagination, but there is no
trace of an invagination at the opposite pole, where four large nuclei can be recog-
nized (Fig. 27 B). The following developmental stages show no trace of a gut.
The apical organ develops further as an invagination and the frontal organ forms
simultaneously as a transversely elongated invagination.
The cilia of the prototroch develop on a ring of large cells below the equator
of the embryo. An area of the epithelium just behind the apical organ comes into
intimate contact with the tissue of the mother animal and a sort of placenta is
formed. A deep furrow forms just above the prototroch cells, and a bud develops
from one side of the bottom of this furrow (Fig. 27E). The differentiation of the
100 IJ
FIG. 26. Loxosomella varians. A narcotized larva seen from above, from below and from the
right side.
organs of the bud (Fig. 27 G) proceeds in the same way as in the normal budding
process described later (see p. 276). The fully grown larva (see Fig. 62) has a prom-
inent frontal organ with a pair of eyes with reddish pigment cups. Its rather small
foot is densely covered with short cilia and bears six large syncilia on the foot
knob. A pair of protonephridia opens lateral to the foot.
The larva has only a short planktonic stage. After about one day the internal
bud ruptures the episphere of the larva and attaches to the substratum with the
well-developed foot (Fig. 27 K). The larval body falls off after some hours and dies.
236 CLAUS NIELSEN
~
~
A
B
c
o
E
F
K
FIG. 27. Loxosomella vivipara. A, eight-cell stage; B, section of a 62-cell stage showing the apical
invagination; C, a median section of a young embryo with a newly formed apical organ; D, a
similar section of a somewhat older embryo; E, an oblique section of the embryo shown in D
showing the primordium of the bud; F, a section showing a further developed bud; G, a section
Loxosoma davenporti Nickerson, 1898

LITERATURE: Nickerson (1901) described a median area of the atrial epithelium
of the mother animal, specialized as a "mammary organ" with very high cells,
some of which may loosen and become ingested by the embryos lying in close con-
tact with this organ.
NEW OBSERVATIONS: A few of the specimens mentioned in an earlier paper (Niel-

sen, 1966b) contained embryos, and the oldest of these resembled the larva of L.
pectinaricola in general shape but was devoid of the characteristic stalked vesicles
on the episphere. Each of the lateral "wings" of the larva showed an oval thicken-
ing of the epithelium resembling early stages of buds.
Loxosoma jaegersteni Nielsen, 1966

LITERATURE: Jagersten (1964) described the larva of this species (the brown type
B larva) from plankton samples. He observed a pair of large buds inside the
larva and followed how they were released through rupture of the dorsal body
wall of the larva. The newborn juveniles were sexually mature males, and Jager-
sten took this as an indication of protandrous hermaphroditism in this species.
Nielsen (1966 a) obtained larvae from the same area and followed the development
of the juveniles to a stage which must be considered adult.
The fully grown larva (see Fig. 73) has a pair of reddish-brown eyes, and a
small cylindrical papilla with a vesicular sense organ at the tip occurs on both
sides of the episphere (Jagersten, 1964, pI. 1, figs 6-7). The larva has a functional
gut and seems to have a long pelagic, planktotrophic existence. The larva dies a
few days after the liberation of the internal buds; no signs of regeneration have
been observed.
Loxosoma okudai Yamada, 1956

LITERATURE: In the original description of this species Yamada (1956) described
and pictured some small stalked organisms which he believed were newly settled
larvae of the same species. An examination of the drawings shows, however,
that the organisms are very small (heads only 60 fL in length) compared with the
of an embryo containing a fully formed bud sectioned in the median plane; H, a transverse sec-
tion of a larva with a fully formed bud; I, a larva seen from above, the internal bud is shown; K,
the internal bud has ruptured the episphere of the larva. From Nielsen (l966a), partially redrawn.
Ap, apical organ; At, atrium of the bud; Bu, early stage of the bud; FG, foot gland of the bud;
FL, foot of the larva; Fo, foot of the bud; Fr, frontal organ; Ga, ganglion of thebud; In, intes-
tine of the bud; Oe, oesophagus of the bud; Po, pore of invagination; Pr, prototroch cells; Re,
rectum of the bud; Ri, ring fold above the prototroch; St, stomach of the bud; Sy, syncilia of
the prototroch; Te, tentacles of the bud.
238 CLAUS NIELSEN
embryos (about 200 [J. in diameter). I presume that the pictured "larvae" are
actually contracted vorticellids, and that the foot gland described in the stalk is
the contractile filament of the vorticellid stalk. There is no indication of a foot
gland in the buds on the adult specimens in Yamada's drawings, and the species,
therefore, belongs to the genus Loxosoma as defined by Mortensen (1911).
Loxosoma pectinaricola Franzen, 1962

LITERATURE: The larva was briefly described in an earlier paper (Nielsen, 1967b).
It has a kidney-shaped prototro ch with a width of about 185 [J. and a length of
about 100 [J. (without the cilia). A group of 10-15 stalked vesicles with a diameter of
5-25 [J. is found on each side of the episphere. There is no ciliated frontal organ. The
hyposphere shows a wide and shallow atrial groove, but there is no trace of a foot.
NEW OBSERVATIONS: This species is very common on the pectinariid polychaete

Pectinaria belgica (Pallas) from muddy bottoms in the northern and middle parts
of the 0resund, depth 25-35 metres. The new material was collected in October-
November 1967-68.
Serial sections of the larva have shown the presence of a pair of lateral sense
organs which had been overlooked earlier (see Figs 28, 30); they are found an-
tero-Iaterally, a little below the group of stalked vesicles.
The apical organ is covered by a thick hyaline cuticle through which the cilia
protrude. A pair of nerves runs from the anterior side of the somewhat bilobed
lower part of the apical organ to a dumbbell-shaped frontal ganglion (Figs 28, 30).
The median part of this ganglion shows only nerve fibres, while about six very
large nuclei are found at each of the lateral swellings. A small transversely elongated
pit with a nucleus at each side apparently represents the epithelial part of the usual-
ly large and highly differentiated frontal organ. A pair of thick nerves proceeds
from the lower lateral parts of the frontal ganglion to the prototroch near the la-
teral parts of the mouth. The nerve fibres can be followed along the basal part of
the large cells of the prototroch (Fig. 31). Just below the frontal ganglion a smaller
nerve is split off from the prototroch nerve and runs in a loop to the lateral sense
organs, which have a swollen basal part with two to three large nuclei and a narrow
cylindrical distal part. There is a small pit with a tuft of cilia at the somewhat
swollen tip of the sense organ.
A pair of powerful muscles originates anterolaterally at the apical organ;
these muscles follow the posterior sides of the nerves via the frontal ganglion al-
most to the prototroch, where they attach to the oesophagus near the lateral parts
of the mouth (Fig. 30). Smaller muscles originate at the cells below the stalked
vesicles and spread along the epithelium of the inner lateral folds. A pair of smal-
ler muscles originates at the posterior part of the episphere behind the basal cells
of the stalked vesicles and has a common attachment at the median posterior
100fJ
apical organ nerve from apical organ
to frontal organ
frontal ganglion
"frontal
lateral sense organ

prototroch constrictor oesophagus ffitractor prototroch nerve
FIG. 28. Loxosoma pectinaricola. Reconstruction of a larva in frontal view showing the most
important nerves and muscles; the stalked vesicles have been omitted.
100~
stomach frontal ganglion
"frontal organ"
intestine
oesophagus
prototroch
rectum
anus
FIG. 29. Loxosoma pectinaricola. A median section of an expanded larva. Camera lucida.
240 CLAUS NIELSEN
o.
100f) small muscles behind frontal ganglion stalked vesicle
frontal ganglion
to lateral sense orqan

oesophagus constrictor
lateral
oesophagus retractor nerve to prototroch small muscles from epi- to hyposphere
FIG. 30. Loxosoma pectinaricola. Transverse section of an expanded larva showing the frontal
ganglion and the lateral sense organs. Camera lucida.
100f) muscle from basal cells of muscles from upper posterior part of episphere
stalked vesicles to inner fold to posterior incurvation of prototroch
outer lateral lateral groove stomach stalked vesicle
inner fold
prototroch constrictor oesophagus
muscles from prototroch cells

prototroch to inner fold prototroch nerve prototroch with ciliary rootlets
FIG. 31. Loxosoma pectinaricola. An almost horizontal section of an expanded larva showing the
frontal part of the prototroch with nerve and muscle. Camera lucida.
c D
FIG. 32. Loxosoma rhodinicola. A-B, a narcotized larva in frontal and lateral views; C-D, a
narcotized larva seen from above and below; E, a contracted larva in frontal view.
point of the prototroch. An unpaired muscle originates at the posterior side of the
apical organ and attaches to the posterior part of the stomach. A powerful muscle
follows the ring of large prototroch cells. All these muscles appear to act in the
contraction of the larva. A number of small muscles between the inner lateral
fold and the prototroch are probably active at the expansion of the prototroch.
The alimentary canal is divided into the four portions characteristic of all
entoprocts. Nephridia have not been observed in the sections or in the living
larvae.
Loxosoma rhodinicola Franzen, 1962

LITERATURE: It was mentioned in an earlier paper (Nielsen, 1967b) that the larva
of this species resembles that of L. pectinaricola.
NEW OBSERVATIONS: Many adult specimens attached to the maldanid polychaete

Rhodine loveni Malmgren were obtained from a muddy bottom between Lysekil
16
242 CLAUS NIELSEN
and Fiskebackskil (Swedish west coast), depth about 50 metres, in August-Sep-

tember 1969.
The fully grown larva (Fig. 32) closely resembles that of L. pectinaricola but
is somewhat smaller, only about 125 flo wide and 100 fl. high when swimming,
and there are only four to seven stalked vesicles in each of the lateral groups.
The apical organ has the usual shape, but a frontal organ has not been observed.
A pair of small bulbous sense organs occurs in front of the groups of stalked ves-
icles. The powerful prototroch is interrupted posteriorly and a complete ring of
small cilia occurs above the prototroch. The hyposphere is ciliated except for a
pair of round areas at the sides of the anus; the cilia encircling these naked areas
are somewhat longer than the other cilia of the hyposphere.
The larva swims rapidly through the water and has been observed to ingest
food, but I have not been able to keep it alive for more than a few days.
Fam. PEDICELLINIDAE
The two families Pedicellinidae and Urnatellidae are, as mentioned earlier, closely
related, and Urnatella is therefore transferred to the Pedicellinidae. They com-
prise colonial species which probably all have the characteristic "star" cell com-
plex at the transition between the calyx and the stalk (Emschermann, 1969; Fran-
zen, 1970b).
The systematics of the Pedicellinidae seems rather chaotic. The largest genus
is Barentsia (including Ascopodaria, Gynopodaria, Arthropodaria, Pseudopedicelli-
na, Pedicellinopsis, and maybe also Coriella). Urnatella seems rather close to
Barentsia. Some of the species within this group seem highly variable, and it
appears necessary to rear a number of species under various conditions to get a
clear impression of the delimitation of the species. The other well-known genus
is Pedicellina, which has recently been revised by Ryland (1965 b); it comprises
about a dozen species. The four remaining genera seem closest to Pedicellina;
Myosoma and Loxosomatoides comprise two species each, while Chitaspis and
Sangavella are monotypic.
Pedicellina cernua (Pallas, 1774)

LITERATURE: The development of this species has been described by a number of
authors, and Cori's (1929) semidiagrammatic drawings of the larva and its met-
amorphosis have been reproduced in almost all later textbooks as representative
of all types of entoprocts.
The embryology has only been studied by few authors. According to Marcus
(1939), the cleavage is almost equal and follows the spiral pattern. At the 56-cell
stage the following arrangement of the cells was observed (Fig. 33 B): 44 ectomeres
arranged as follows: 4 smaller apical cells (1 a 111 - 1d 111), 8 larger cells in a ring be-
low the apical cells (1 am - 1d l12 and 1a 12l - 1d I 2 I ) , 12 medium-sized cells forming
A B c
ao
50 IJ
F
FIG. 33. Pedicellina cernua. A, eight-cell stage; B, 56-cell stage, the 4d cell is dotted; C, a median
section of a gastrula; D, a median section of a somewhat later stage; E, an optical section of an
embryo showing apical and frontal organs; F, a median section of an embryo in which the foot
is forming. A-D, F redrawn from Marcus (1939), E redrawn from Hatschek (1877); ao, apical
organ; f, foot; fa, frontal organ; oe, oesophagus; p, proctodaeum; s, stomach.
a rather narrow ring just above the equator of the embryo (1aU' - 1d 122 , 1a 21 -
1d· l and 1a 22 - 1d 22 ) , and below that a somewhat irregular ring of 20 cells of dif-
ferent sizes (2a ll - 2d ll , 2a l ' - 2d u , 2a' 1 - 2d 21 , 2a 22 - 2d 22 and 3a - 3d); the
large and rounded 4d cell, which is somewhat displaced into the interior of the
blastula, which has a small blastocoele; and finally, 11 entomeres of somewhat dif-
ferent sizes (4aAc, Sa-Sd and 5A-SD). The cell lineage has not been followed
beyond this stage. The descriptions of Barrois (1877, as P. echinata) and Hatschek
(1877, as P. echinata) are not in complete agreement with the above statements
and their drawings of embryos of corresponding stages generally show fewer cells
than Marcus' drawings. The earlier authors did not use serial sections and this
may have given rise to some misinterpretations. Marcus' description is, therefore,
followed when nothing else is stated.
The gastrulation starts at a stage of about 120 cells. It takes place through in-
16'
244 CLAUS NIELSEN
vagination and the opening of the narrow archenteron becomes blocked by a few
small cells of uncertain origin (Fig. 33 C). The stomodaeum originates from a
thickening of the epithelium just in front of the blastopore, at a stage of about
200 cells. The 4d cell has divided several times and given rise to the rather scat-
tered mesoderm cells. Some few ectomesenchyme cells are given off from the
borders of the stomodaeum.
The apical organ and the frontal organ differentiate from thickenings of the
ectoderm (Seeliger, 1906), and the proctodaeum originates as a small invagination
from the epithelium behind the stomodaeum (Fig. 33 E). The embryo has at this
stage developed a distinct ring furrow which lies just above the cells of the pre-
sumptive prototroch (Hatschek, 1877). At this stage the membrane surrounding
the embryo disappears except for the stalk and a ring around the apical organ.
The frontal organ has at one stage a lumen in the shape of a forked canal with
cilia, indicating that the organ was originally paired (Czwiklitzer, 1909, pl. 1,
fig. 6). The development of the nerves and muscles has not been studied.
A small invagination of thickened epithelium in front of the anus gives rise to
the peripedal groove with the large foot (Fig. 33F). The development of the foot
glands has not been followed, but Marcus (1939, p. 250) states that they are in
contact with the ectoderm and considers them of ectodermal origin. The develop-
ment of the nephridia has not been studied.
The first, rather primitive descriptions of the fully grown larva were given by
Reid (1845, as P. echinata) and Gosse (1853, as P. belgica). Later on Uljanin (1869,
as P. echinata), Hincks (1873, as P. belgica), and Barrois (1877, as P. echinata)
gave more detailed descriptions of its morphology. Hatschek (1877, as P. echinata)
published a very well-illustrated description of the embryology and the fully
grown larva.
The just-mentioned authors did not observe the settling of the larva and had
to propose various theories concerning its metamorphosis. Finally, Barrois (1881)
observed the metamorphosis and stated that the larva settles with the "oral pole",
and that the alimentary canal undergoes a 180 0 rotation. These observations are
also mentioned in two later publications (Barrois, 1882, i886), in the last-mentioned
case illustrated by some rather diagrammatic drawings.
Harmer (1886) gave a thorough histological investigation of the metamorphosis
and Prouho (1892) described some details of the fully grown larva.
Lebedinsky (1905, as P. echinata) described the fully developed larva but mis-
interpreted the three pairs of foot glands as somites containing the excretory and
reproductive organs. Several ganglia not found by other investigators were also
described. These findings are excluded from the following discussion.
Seeliger (1906, as P. echinata) gave rather detailed descriptions of the nerves
and muscles. Both the text and the figures indicate the presence of cilia in the pe-
ripedal groove but none in the atrial groove; this is contrary to what has been found
by all other investigators.
Czwiklitzer (1908) gave a detailed description of the apical and frontal organs
and their nerves, based on sections of fully grown larvae which had been narcotized
with cocain and which, therefore, could be fixed in the expanded state. He also
described the foot glands and was the first to interpret them correctly.
The well-known schemata of the metamorphosis of the Pedicellina larva were
drawn by Cori (1929).
Finally, Marcus (1939) made a thorough study of the whole embryology and
discussed his own findings in relation to the earlier literature.
The observations of these authors on the larvae can be summarized as follows:
The fully grown larva (see Fig. 62) has an oval prototroch which is a little longer
than wide. It has a prominent apical organ with a central area with single cilia
and a peripheral ring of small "tentacles", each with a tuft of cilia. The frontal
organ has an unpaired ciliated knob. The episphere is usually covered by scattered
"detritus" particles. A few sensory bristles occur in a symmetrical pattern on the
episphere. In the swimming larva there is a deep infolding just over the prototroch,
and above the posterior part of this is another, more shallow, infolding. These in-
foldings become straightened out when the larva contracts. The prototroch con-
sists of a row of cells with large syncilia. The oral groove is wide and ciliated and
the posterior part of the peripedal groove has a thick epithelium with large nuclei.
The foot is ciliated on the sole and there are a number of large syncilia on the foot
knob. The alimentary canal shows the usual four regions: oesophagus, stomach,
intestine and rectum, and the anus opens on the posterior part of the sole of the
foot. The protonephridia have been observed as a pair of narrow ciliated ducts
on either side of the foot. There are three pairs of large glands along the foot: the
first and third pairs are filled with oval droplets which stain intensely with haem a-
toxylin; the second pair shows a peculiar reticulate pattern in the sections and has
pycnotic nuclei. The apical and frontal organs are connected by a pair of nerves
accompanied by muscle fibres. A pair of nerves proceeds from the lateral part
of the frontal organ to the foot knob. Several authors mention a suboesophageal
ganglion in this region but none of their drawings indicate the presence of a
structure of this sort. Czwiklitzer (1909) observed a pair of small nerves running
from the lower side of the frontal organ to the prototroch.
After a short free period the larva selects a substratum and initiates the meta-
morphosis as described by Harmer (1886). The apical and frontal organs and the
whole hyposphere retract and the larva attaches to the substratum by means of
the cells above the prototroch. The peripedal rim ("lateral fold of vestibular wall")
constricts almost completely below the contracted foot, whose cells separate and
start disintegrating. Some of these loose cells can later on be found in the stomach
of the young specimen. It is not explained clearly how the "bottom" of the atrium
forms.
0
The gut undergoes a 180 rotation in the median plane, with the mouth first.
The closed mouth region (or perhaps a part of the "oral" division of the vestibule)
246 CLAUS NIELSEN
FIG. 34. Pedicellina cernua. A median section of an expanded larva.
comes into contact with the space above the constricted peripedal rim (the "anal"
division of the vestibule) from which the tentacles develop as a double row of epi-
thelial thickenings. The mouth forms as an opening through the septum between
the oesophagus and this space. Finally, the cuticle above the tentacles bursts and
the atrium reopens. Nothing is stated about the origin of the ganglion or the pro-
tonephridia.
NEW OBSERVATIONS: Many colonies containing larvae were collected from various
types of bottoms at Stangholmen, Byxeskar and Flatholmsskaran (the Gullmar-
fjord, Swedish west coast), depths 16-40 metres, in August-September 1969.
Only a few additions to the above description can be given and the photographs
of some sections illustrate the development (Figs 34-39).
The larva has a ring of small cilia above the large syncilia of the prototroch.
In younger stages of the metamorphosis it is often possible to observe large
cells with a tuft of enclosed cilia still beating slowly (Fig. 37). These cells are es-
FIG. 35. Pedicellina cernua. A median section of a strongly contracted larva.
,--- -
thickenedepithetil;Jm
of peri pedal groove'
FIG. 36. Pedicellina cernua. A median section of a newly settled larva.

248 CLAUS NIELSEN
100 ~
FIG. 37. Pedicellina cernua. A newly settled

larva; a protonephridium and five cells con-

taining slowly beating cilia are indicated.
pecially easy to observe at the sides of the oesophagus. Comparisons with the serial
sections have shown that these cells are degenerating cells from the foot knob.
The origin of the epithelium covering the bottom of the atrium in the adult has
been difficult to make out. It is clear that the largest part originates from the
thickened epithelium of the sides of the foot (= the posterior lateral part of the
peripedal groove) and it is my impression that the edges of this epithelium constrict
intestine
stomach
oesophagus
FIG. 38. Pedicellina cernua. A median section of a specimen which has carried through part of
the metamorphosis; about 90° of the rotation of the alimentary canal has taken place.
cells containing
degenerating cilia
FIG. 39. Pedicellina cernua. A median section of a specimen which has almost completed the
metamorphosis; the atrium is still covered by the cuticle.
250 CLAUS NIELSEN
totally below the foot. The whole epithelium of the atrium and the tentacles seems
thus to originate from the epithelium of the peripedal rim.
The ganglion originates from a transversely elongated thickening of the ecto-
derm between the mouth and the rectum. The protonephridia develop between the
ganglion and the mouth. The anus breaks through at a late stage.
Pedicellina nutans Dalyell, 1848

TAXONOMY: The species within the genus Pedicellina are very difficult to distin-
guish due to lack of precise characters (Ryland, 1965b). Especially the two Eu-
ropean species P. cernua and P. nutans have apparently often been confused. Ry-
land (1961, 1965b) gave new information on the size and shape of P. nutans and
200 IJ
FIG. 40. Pedicellina nutans.

A, an adult specimen with a
large embryo (dotted) in the
atrium; B-D, a creeping
larva seen from below, from
D
the left side and from above.
FIG. 41. Pedicellina nurans.
A, a rather newly settled
larva, the alimentary canal
has rotated about 90°; B, a
small specimen which has
just opened the atrium after
the metamorphosis; D, a
fully formed specimen four
days after the settling of the
larva.
c ' I
J
<, J
pointed out that the two species probably can be distinguished by differences in
maximum size, tentacle number and shape of the anal cone.
My material of Pedicellina from Danish and Swedish waters clearly comprises
two species. One has the characteristic lobulate brood pouches pictured by Cori
(1936, fig. 48) and a larva which closely resembles that described by Hatschek
(1877), Czwiklitzer (1909) and Marcus (1939). This species fits the descriptions of
P. cernua well and is treated above under that name. The other species (Fig. 40A)
grows luxuriously on algae, hydroids, shells, etc., at a depth of 0-1 metre on the
breakwaters of Frederikshavn harbour (northern Jutland). It attains a total length
of up to 4.5 mm (including tentacles) and has 12-16 tentacles. The stalk lacks spines
and tapers gently upwards. Specimens without embryos have only slightly asym-
metrical calyces, and their anal cones are almost horizontal. The most charac-
teristic feature is, however, the enormous larva (Fig. 40B-D) which creeps on the
252 CLAUS NIELSEN
FIG. 42. Pedicellina nutans. A median section of a larva.
substratum and is unable to swim. Probably as a consequence of the size of the larva
no lobulate brood pouches are found. Although the specimens attain a size which
is far above that previously reported for P. nutans, they resemble this species in
most respects, and Dr. J. S. Ryland (Swansea) is of the opinion that it is an ex-
tremely well-developed type of this species. A branch of a colony from Frederiks-
havn has been pictured as P. cernua by Nielsen (1964, fig. 39).
NEW OBSERVATIONS: Many specimens of the colonies collected at Frederikshavn

(see above) in June-July 1968-70 contained one or two large embryos in the atrium,
and several larvae were soon released.
The larva is very characteristic (Fig. 40B-D). It is up to about 350 fl. long and
about 280 fl. wide. The episphere is strongly folded, as if the skin is "too large"
for the animal; the pattern of the folds shown in the drawing was found in almost
all the specimens. The apical organ is not very prominent. The frontal organ is
almost circular and has a strong ciliation. A number of stiff sensory bristles are
scattered over the episphere. There are no "detritus" particles adhering to the larva.
FIG. 43. Pedicellina nutans, A transverse section of a larva; the foot curves forwards.
The prototroch has rather small cilia (Fig. 43) and the larva is unable to swim.
The atrial groove and the foot show the usual ciliation and there are about fifteen
syncilia on the foot knob.
Serial sections (Figs 42, 43) show that the anatomy of the larva corresponds
closely to that of P. cernua.
After one to a few days of creeping the larva selects a place to settle. It creeps
in small circles or rotates slowly on the same spot, "testing" the substratum with
the protruded frontal organ. Finally, the prototroch contracts and the larva now
sticks firmly to the bottom. Observations on live material and sections of various
stages of the metamorphosis have shown that this process takes place in exactly the
same way as in P. cernua (Fig. 41). The atrium reopens about four days after the
larva has settled.
254 CLAUS NIELSEN
FIG. 44. Sangavella vineta. Left view of a young

larva dissected out from the atrium of the
mother animal.
50 fJ
Sangavella vineta du Bois-Reymond-Marcus, 1957

NEW OBSERVATIONS: A colony growing on a fragment of a parchment-like tube
probably built by a polychaete is kept in the Zoological Museum, Copenhagen.
The sample has been identified by Dr. E. du Bois-Reymond-Marcus and was col-
lected at Pereque Beach, Guaruja, Ilha de Santo Amaro, State of Sao Paulo,
Brazil, by Mr. O. Alexandre, 23 November 1958.
Large embryos (Fig. 44) could be obtained from several calyces. Their general
shape resembles that of the larvae of Barentsia gracilis A, but a series of sections
definitely shows that a frontal organ is not developed; a frontal ganglion seems to
be present. There is a pair of strong retractor muscles connecting the lateral parts
of the apical organ with the sides of the oesophagus. There is no trace of a foot,
and although the foot develops late in Pedicellina cernua I hardly believe that a
foot develops in the larva of Sangavella. The state of fixation of the sample does
not permit a more detailed study.
Barentsia benedeni (Foettinger, 1887)

LITERATURE: The larva (see Fig. 62) was figured by Toriumi (1944) but no descript-
ion was given. The larva resembles that of B. taxa.
Barentsia discreta (Busk, 1886)

TAXONOMY: The delimitation of this species is somewhat uncertain, but the ma-
terial treated below closely resembles the specimens described by Busk (1886) and
Harmer (1915). B. macropus (Ehlers, 1890), described from the Spanish coast of
the Mediterranean, is by some authors (e. g., Rogick, 1956a) considered identical
with B. discreta. Prenant & Bobin (1956) and Maturo & Schopf (1968) considered
100 ~
500 ~
FIG. 45. Barentsia discreta. A, an adult specimen from Naples; B, a swimming larva seen from
the right side; C, a newly settled specimen; D, a specimen which has just opened the atrium
after the metamorphosis.
256 CLAUS NIELSEN
B. macropus a valid species, and referred the specimens found on Posidonia from
Naples (Zirpolo, 1928, as B. discreta) to that species. My material (see Fig. 45A)
was likewise found on Posidonia from Naples and a comparison with the descrip-
tions given by the authors mentioned clearly shows that my material at least pro-
visionally must be treated under the name B. discreta. The most characteristic
features of the species are that the long rigid portion of the stalk is unjointed,
unbranched and bears so-called pores and that its diameter increases upwards.
LITERATURE: Ehlers (1890, as Ascopodaria macropus) pictured a newly liberated

larva (op. cit., fig. 101), but the drawing is rather schematic and according to my
experience shows a larva which has been liberated too early.
NEW OBSERVATIONS: Several colonies were found growing on Posidonia from a

depth of 12-20 metres, near Posillipo (Bay of Naples), in May-June 1967.
Several specimens had embryos in the atrium and larvae soon were liberated.
The swimming larva (Fig. 45B) is about 190 flo high and has an almost circular
prototroch with a diameter of about 125 flo (without the cilia). There are no par-
ticles adhering to the episphere. The apical and frontal organs and the whole di-
gestive tract resemble those of the larva of B. gracilis A. In the swimming larva
only the tips of the syncilia of the foot knob protrude below the inner edge of the
atrial groove. The rectum is unusually voluminous and it is not possible to dis-
tinguish a foot in the swimming larva.
The larvae usually settled after less than one day. They became attached by
means of the cells above the contracted prototroch. The metamorphosis took place
in the same way as described for B. gracilis B (Fig. 45 CoD). The atrium reopened
about five days after the larva had settled and at that stage the diffentiation of the
stalk into a muscular basal portion and a non-muscular distal portion could easily
be seen.
Barentsia gracilis (M. Sars, 1835)

LITERATURE: Van Beneden (1845, as Pedicellina belgica) observed a few stages of
the development of this species and also gave a description of the external mor-
phology of the larva. More recently, Cori (1936) gave a drawing of a large larva
still attached to the embryophore of the mother animal; this larva resembles that
of Pedicellina cernua.
Mariscal (1965) described the adult larva and gave a drawing of a para-median
and a transverse section; these drawings generally agree with Czwiklitzer's (1906)
description of the Pedicellina larva. Mariscal pointed out that the larva resembles
the adult so much that the rotation observed at the metamorphosis of the Pedicel-
lina larva "seems completely unnecessary". His drawings of the larva show a pair
of rather thick nerves running from the apical organ to a "subenteric" ganglion
between the stomach and a pair of large foot glands; other nerves connect this
ganglion with the foot glands, the corona and various parts of the epidermis.
Protonephridia were not observed, but "a clear unpaired tubular structure, which
ends in a thin-walled rounded pocket at the edge of the vestibular groove" (op.
cit., p. 323) was interpreted as possibly representing an early developmental stage
of a nephridial canal. These unexpected findings will be discussed below. It was
observed that the cilia of the atrial groove carry particles to the mouth and that
particles to be rejected are carried backwards along the edge between the atrial
and peripedal groove. It was also observed that the larvae "steal" food particles
from the vestibular groove of the mother animal.
I
NEW OBSERVATIONS: Many colonies bearing larvae were obtained from localities
in the vicinity of the Kristinebergs zoologiska Station (Swedish west coast), especial-
ly from Gaso Ranna and around Byxeskar, depth 30-40 metres, in August-Sep-
tember 1969 and 1970. The colonies grew on shells of Buccinum, Turritella and
Aporrhais inhabited by Phascolion or Pagurus, on hydroids and on pieces of oilskin.
The larvae released from these colonies were of two quite different types which
could be recognized even while the larvae were still in the atrium of the mother
animal. In no case were larvae of both types found in one mother animal or in
mother animals on the same stolon, although mother animals containing the two
types of larvae were often found to grow between each other. It was on this back-
ground tempting to regard the two types as separate species, but I have been un-
able to find reliable distinguishing characters between colonies producing the two
types of larvae. Dr. P. Emschermann (Freiburg/Breisgau, Germany) has kept
colonies of both types in culture and has informed me that the vague differences
which I had believed to exist between the two types of colonies are not constant.
I have, therefore, decided provisionally to treat the two types as B. gracilis types
A and B. The larvae described by Cori (1936) and Mariscal (1965) come closest
to the type B larva.
Type A
The larvae (and the large embryos) of this type are very characteristic, their whole
episphere being covered with a dense layer of small whitish particles which make
the larvae quite opaque; most of these particles dissolve in Bouin's fluid. The
swimming larva (Fig. 46 A-C) has an almost circular prototroch with a diameter
of about 120 fL (without the cilia) and is about 160 fL high. The apical organ is
usually strongly protruded and has a ring of small clavate tentacles around the
periphery and rather long cilia at the central part. The frontal organ is rather small;
sections have shown that it has a central cavity, but cilia have not been observed.
There is a deep infolding around the episphere, only interrupted below the frontal
organ. The layer of particles of the lowermost part of the episphere can be seen
through the cells of the expanded prototroch. There is a ring of small cilia above
the large syncilia of the prototroch; both rings are interrupted posteriorly. The
17
258 CLAUS NIELSEN
A c
100 ~
D E
FIG. 46. Barentsia gracilis A. A-C, a swimming larva, in frontal, posterior and left lateral views; D,
a, strongly contracted larva in left lateral view; E, the same specimen after fixation in Bouin's fluid.
hyposphere has a rather uniform ciliation. There is no trace of a foot, but a pair
of small invaginations slightly anterior to the anus are bordered by cells with
granular cytoplasm; these formations may either represent the primordia of the
foot or the primordia of the foot glands. The contracted larva (Fig. 46 D-E) is
very high and narrow. The configuration of the internal organs corresponds to
that of other larvae of the Pedicellinidae.
Larvae have been kept alive in small dishes with pieces of natural substratum
for up to eleven days; during the first days they kept swimming, but later on they
were creeping most of the time. None of the larvae settled.
100 fJ
c D
FIG. 47. Barentsia gracilis B. A-B, a narcotized larva, in frontal and left lateral views; C, a
strongly contracted larva seen from the left; D, a newly settled larva.
TypeR
The larvae of this type have only very few "detritus" particles on the episphere,
and the brown stomach can easily be seen through the body wall. The swimming
larva (Fig. 47 A-B) has an oval prototroch with a length of about 125 !l. and a
width of about 100 !l. (without the cilia). The episphere is domed, with prominent
apical and frontal organs, and bears a few scattered sensory bristles. The proto-
troch consists of strong syncilia and there is a row of smaller cilia above it; both
rows are interrupted posteriorly. The hyposphere shows the ciliated atrial groove
and a foot which is ciliated on the "sale" and on the sides of the foot knob,
which bears about ten large syncilia. The contracted larva (Fig. 47 C) is about as
long as wide, which is in strong contrast to the shape of the type A larva (see
17"
260 CLAUS NIELSEN
FIG. 48. Barentsia gracilis B. A, a specimen which has carried through part of the metamor-
phosis; B-C, a specimen which has almost completed the metamorphosis, in lateral and frontal
views; D, a specimen which has recently opened the atrium and in which the differentiation of
the stalk has begun.
-r-f",,-'t---- apical organ
second pair of
foot glands frontal organ
protonephridium -~~3f-l"~~~?C>?::
third pair of pair of

foot glands glands
FIG. 49. Barentsia gracilis B. A reconstruction of a larva showing the apical and frontal organs
(dotted), the alimentary canal, the most important nerves (dotted), and the three pairs of foot
glands (compare with Fig. 50).
FIG. 50. Barentsia gracilis B. An almost median section of an expanded larva.

262 CLAUS NIELSEN
100 ~
nerve from frontal organ

frontal organ
to foot knob
oesophagus
1'":""--- atrial groove
:.~
--,."~-:,,"".'.'.~
-, mouth
peripedal groove foot knob
FIG. 51. Barentsia gracilis B. Section no. 17 of a series of transverse sections of an expanded larva.
100 IJ
atrial
peri pedal rim foot "sole"
groove
t.hickenedepithelium of peripedal gro.ove
groove
peripedal
FIG. 54. Barentsia gracilis B.Section no. 32 of series of transverse sections of an expanded larva.
264 CLAUS NIELSEN
degenerating·
apical_ organ
oesophagus
FIG. 55. Barentsia gracilis B. An almost median section of a newly settled specimen.
Fig. 46D-E). The creeping larva often protrudes the frontal organ strongly and
presses it against the substratum.
One median and four transverse sections of expanded larvae illustrate the
anatomy (Figs 50-54). The external surface of the apical organ is covered by a
hyaline cuticle which is pierced by cilia and shows a peripheral ring of small
club-shaped papillae, each with a small tuft of cilia at the end. From the lower
lateral parts of this organ two short nerves run to the apparently unpaired frontal
organ. From the sides of the frontal organ a pair of nerves runs lateral to the
oesophagus, just in front of the frontal foot glands, and spreads its fibres in the
foot knob.
The alimentary canal shows the four regions characteristic of all adult ento-
procts. The anus lies on the "sole" of the foot near its posterior end. The glands
of the foot (Fig. 49) are of two types; the second pair has a finely granular cyto-
plasm with pycnotic nuclei, while the first and third pairs are almost totally filled
with ovoid droplets of secretion. The epithelium of the posterior part of the peri-
pedal groove consists of cells with large nuclei with conspicuous nucleoli.
Many scattered muscles connect the foot, the walls of the oesophagus and the
atrial groove with the upper part of the episphere. A conspicuous pair of these
muscles runs from the middle of the foot along the median sides of the second
pair of foot glands to the upper part of the episphere (Fig. 53). These muscles are
probably the most important retractors of the foot. Together with some of the
FIG. 56. Barentsia gracilis B. A median section of a specimen which has carried through part of
the metamorphosis; the alimentary canal has rotated about 90°.
retractors of the atrial groove, their configuration resembles the system of "nerves"
described by Mariscal (1965, fig. 9). I have, however, neither been able to find any
fibres connecting the region below the stomach with the apical organ, nor to find
any structure below the stomach resembling a ganglion. I therefore assume that
the subenteric ganglion and the connecting nerves described by Mariscal must
be misinterpretations. (It may be added that nerves and muscles are difficult to
distinguish in the sections, and that it seems worth while to make a more detailed
study of the nerves and muscles of this larva.) A pair of protonephridia (Fig. 54),
each consisting of three cells, is found lateral to the posterior part of the median
foot glands, opening into the peripedal groove. The lower lip gland described by
Mariscal (1965, fig. 8) has not been observed, but may represent a misinterpre-
tation of the anterior part of the peripedal groove (Fig. 50).
The larvae may swim and creep for a period of a few hours to a few days before
they settle. When a suitable place has been selected the larva contracts with the
upper edge of the contracted prototroch in contact with the substratum. Sections
of newly settled larvae (Fig. 55) show that the large foot glands have disappeared
totally and this supports the theory that they provide the secretion which glues
the larva to the substratum. Such sections also show that the ciliated cells of the
foot separate and become laterally displaced; at this stage there is thus no epithe-
lium separating the wall of the stomach from the lumen of the atrium. The retracted
266 CLAUS NIELSEN
FIG. 57. Barentsia gracilis B. An almost median section of a specimen which has almost com-
pleted the metamorphosis; the atrium is still covered by the cuticle.
apical and frontal organs start to disintegrate, but can still be distinguished dur-
ing some of the following stages.
The peri pedal rim closes below the retracted foot and the atrium thus becomes
divided into two compartments. During the following development the mouth
constricts and the lower compartment of the atrium with the cilia of the prototroch
disintegrates (Fig. 56).
The epithelium of the posterior part of the peripedal groove, which already in
the larva appeared very active, with large nuclei, now starts to grow rapidly. Its
median edges along the sides of the foot fuse and the epithelium of the median part
of the groove thus comes to form the ectodermal cover of the stomach: this epi-
thelium differentiates further during the following development and comes to
cover the whole atrium of the adult. The lateral edges of the peripedal groove
(the peripedal rim) are likewise fused and the epithelium of the lateral sides of the
groove later on differentiates into the epithelium of the tentacles. By the well-known
0
180 rotation of the whole alimentary canal the oesophagus of the larva comes
into contact with this flattened epithelial sac formed by the epithelium of the peri-
pedal groove, and a mouth opening forms. This rotation is accomplished within
about half a day.
Already before the rotation is completed a short stalk region can be recog-
nized (Fig. 48A). This region elongates and muscle fibres are already differen-
tiated about three days after the settling.

The stalk is filled with large cells containing strongly refractive vacuoles, and
degenerating cilia can be recognized in many cells. At the stage pictured in Figs
56 and 57 the ganglion has already been formed as a small, laterally elongated
thickening of the epithelium above the stomach. The developing tentacles can be
seen as elongated thickenings at each side of a narrow median slit, which is seen
in the photograph (Fig. 57). The cuticle still covers the opening of the atrium.
After about one more day the differentiation of the stalk into the basal muscular
part and the upper elastic part begins and the peculiar circulatory organ at the top
ofthe stalk (Emscherrnann, 1969) is formed (Fig. 48D). The cuticle above the atrium
bursts, but the small tentacles are still too little developed to be stretched out.
Barentsia kovalevskii (Nasonov, 1926)

LITERATURE: In the original description of this species, Nasonov (1926) gave a
short description and a rather primitive drawing of the free-swimming larva. The
larva seems to resemble that of B. gracilis Band Pedicellina cernua. Nasonov also
stated that the larva settled after about one day in the same way as that of Pedi-
cellina.
Barentsia laxa Kirkpatrick, 1890

LITERATURE: Rogick (1948) observed embryos and larvae in her material from
Woods Hole. Several embryos occurred at one time in the atrium of the mother
animal and it was observed that the larvae started food uptake before they were
released. The description and drawings of the free-swimming larvae correspond
rather well with my own observations on larvae from Frederikshavn (see below),
although the Danish larvae were somewhat larger and usually had fewer particles
on the episphere,
NEW OBSERVATIONS: A very fine growth was found on an old Laminaria frond
from about 1 metre's depth at the tip of the southern breakwater of the Frederiks-
268 CLAUS NIELSEN
FIG. 58. Barentsia laxa. An adult specimen from

Frederikshavn.
havn harbour, 6 June 1969. The adult specimens

(Fig. 58) closely resembled those described by
Rogick (1948), the only apparent difference being
that my specimens lack the septum at the upper
end of the muscular base. Some of the multilo-
cular resting bodies described by Emschermann
(1961) and Franzen (1970b) were observed.
Many of the specimens contained up to six
embryos, and larvae were released soon after the

isolation of the colony. The fully grown larva
(Fig. 59) is rather large, about 180 [J. long and
x 150 [J. broad when swimming. The posterior part
of the episphere is strongly folded. The episphere
does not seem to be sticky and the irregular
cover of particles so characteristic of several
other larvae has not been observed. The apical
and frontal organs are well developed and re-
semble those of the Pedicellina cernua larva; this
is also true for the details of the prototroch and
50U ~
the whole ciliation of the hyposphere. There are
about ten syncilia on the foot knob. A short
ciliated "tentacle" is found just behind the po-
sterior side of the foot (Fig. 59 D).
The larva swims rapidly through the water,
but starts creeping when it bumps against a firm
object or the water film. The creeping larva often
x
protrudes the frontal organ strongly and "tastes"
the substratum with it. After a period of creep-
ing the larva attaches by means of the upper
side of the contracted prototroch and the meta-
morphosis proceeds in the same way as that of Pedicellina cernua and Barentsia
gracilis B (Fig. 60). The atrium reopens after about four days and eight tentacles
are present at this stage. The differentiation of the stalk into the basal muscular
part and an upper non-muscular part is clearly seen one day later (Fig. 60D).
100 fJ
c o
FIG. 59. Barentsia taxa. A, a narcotized larva seen from the left; B, a narcotized larva in frontal
view; C, a narcotized larva seen from below; D, the posterior part of the lower side of a speci-
men which has the foot curved forwards so that the small tentacle can be seen.
Urnatella gracilis Leidy, 1852

LITERATURE: Emschermann (1965 a) observed that the eggs develop inside the ova-
rium. The large embryos resemble the larvae of the Pedicellinidae in general. The
digestive tract has the normal shape and a small apical and a small unpaired frontal
organ were also observed. The hyposphere is very small but may well grow and
differentiate further before the larva is liberated. Two large flame cells occur on
each side of the embryo.
270 CLAUS NIELSEN
FIG. 60. Barentsia laxa. A, a newly settled larva; B, a specimen which has carried through part
0
of the metamorphosis, the alimentary canal has rotated about 90 C, a specimen which has
;
almost completed the metamorphosis; D, a specimen which has recently opened the atrium and
in which the differentiation of the stalk has begun (four days after the settling).
SURVEY OF ENTOPROCT LIFE-CYCLES

Embryology
The fertilization has not been observed directly, but Marcus (1939) found that in
Pedicellina cernua the egg becomes fertilized already in the ovary. This is probably
the case also in other species which brood the embryos, so that the spermatozoa
need not penetrate the tough membrane which in most species is secreted while
the egg passes through the oviduct. The fertilization is, of course, also internal in
the viviparous species.
In the oviparous species the embryos are generally attached with a string-shaped
elongation of the surrounding membrane to an area of columnar epithelium in

front of the opening of the reproductive organs. The weak membrane soon disap-
pears on Loxosomella leptoclini, in which the embryos are nourished directly by
a special placenta-like area of the lateral brood pouches (Harmer, 1885). The
large larvae of Loxosoma davenporti adhere to the gland-like embryophore ("mam-
mary organ") of the mother animal, but the membrane is present in the early stages
(Nickerson, 1901).
The development has only been studied in few species but that of the most
thoroughly studied species, Pedicellina cernua, fortunately seems to represent a
rather generalized type within the group.
Pedicellina cernua has spiral cleavage, which seems to be found in most species.
The further development follows the pattern found in most trochophore larvae.
In Loxosomella vivipara the eight-cell stage shows the spiral pattern, but the la-
ter stages show no regular arrangement of the cells. A small invagination has been
observed at a stage of 62 cells, but this invagination represents the apical organ;
no trace of a gastrulation has been observed and the larva totally lacks a gut.
The apical organ is well developed in all the larvae investigated so far, but the
frontal organ is very small or lacking, for example, in the larvae of Loxosoma
pectinaricola, Loxosomella elegans and Sangavella vineta. In larvae lacking a fron-
tal organ there is apparently always a small dumbbell-shaped ganglion resembling
the ganglionic part of the well-developed frontal organs of other larvae. This may
indicate that the frontal organ was present in the ancestral type (see later).
Probably all the fully developed larvae have a prototroch consisting of a ring
of large syncilia and above that a ring of small cilia. An area of smaller cilia (adoral
cilia) surrounds the mouth and stretches along the sides of the episphere below
the prototroch; this area usually forms a shallow groove (the atrial groove). In
the larvae which take up food, particles are caught by the prototroch and trans-
ported to the mouth by the adoral cilia. Some larvae lack a foot completely and
show only a ciliated area running from the median part of the adoral ciliary area
towards the anus (e. g., Loxosoma pectinaricola and Loxosomella elegans). Most
larvae, however, have a well-developed foot surrounded by a peripedal groove
272 CLAUS NIELSEN
devoid of cilia. The foot has a ciliated "sole" and its somewhat swollen frontal
part (the foot knob) is ciliated all over and bears a transverse row of large syncilia.
The larva of Loxosomella vivipara totally lacks a gut, but in the other species
the digestive tract shows the very same divisions and the same functions as that
of the adult gut (Becker, 1937). The anus opens on the upper side of the posterior
part of the foot in the Loxosomatidae, but on the posterior part of the "sole" of
the foot in the Pedicellinidae.
The larvae of some species metamorphose and their alimentary canal directly
becomes the alimentary canal of the adult. In other species the budding which
occurs in all the adults starts already in the larva and in these cases the larval body
disintegrates after having given off the buds.
The most primitive type appears to be that which has a regular metamorpho-
sis (Fig. 61). In the Loxosomatidae this type is known to occur in a number of
species of Loxosomella, viz., L. harmeri, L. murmanica.L, crassicauda, and probably
L. varians. The larvae of these species have a well-developed frontal organ and foot.
At the settling they become attached to the substratum with the contracted frontal
organ, probably by a secretion from the row of cells encircling the opening of the
organ. A ring of cells above the prototroch constricts completely below the retrac-
ted hyposphere. The ciliated epithelium of the foot disintegrates completely and the
epithelium of the postero-lateral sides of the foot (the postero-median part of the
peripedal groove) forms the new bottom of the atrium, covering the stomach. The
adoral ciliation and the prototroch disintegrate and the same applies to the frontal
and apical organs and probably to the larval protonephridia. The ganglion of the
adult originates as a transversely elongated thickening of the atrial epithelium
between the mouth and the anus. During these processes the alimentary canal
rotates 90 in the median plane, with the mouth first. The tentacles develop as a
0
row of paired thickenings of the epithelium along the median line of the atrial wall
opposite the stomach. Finally, the cuticle covering the atrium bursts and the small
tentacles, already with well-developed cilia, stretch out.
There is an even transition from. the just-mentioned type to the types in which
the larvae give off buds and die.
In Loxosomella polita the larva settles with the frontal organ and retracts the
hyposphere; the first bud develops at an early stage of the metamorphosis and it
appears that the larval body in most cases dies when it has given off the bud. In
some cases small individuals with degenerating eyes have been found but they
have had quite short tentacles and it is clear that they will never develop the "foot"
characteristic of the adults of this species.
The larva of Loxosomella leptoclini does not settle permanently; it contracts
with the foot in contact with the substratum and develops a pair of lateral buds
(Fig. 61). The larva dies after the liberation of the buds. In some species the buds
develop in epithelial invaginations from the episphere of the larva and disrupt the
larva when they have reached a certain size (Loxosoma jaegersteni). The most
Loxosomella harmer; Loxosomella leptoclin; Loxosomella vivipara
FIG. 61. Developmental types within the genus Loxosomella; the buds are dotted.
specialized type is found in Loxosomella vivipara, in which the larva does not show
any trace of a digestive tract and the single internal bud fills the whole larva
(Fig. 61).
I believe that all species of the genus Loxosoma have life-cycles similar to that
described for L. jaegersteni. It seems quite improbable that the sucker-shaped ad-
hesive organ characteristic of the genus should be formed by the metamorphosis of
the larva. It also appears that the species of Loxosomella in which the adults have
a differentiated "foot" must belong to one of the modified types described above.
18
274 CLAUS NIELSEN
Loxosomella murmanica
Loxosomello harmeri Loxosomella crassicauda
Loxosomella secure
Loxosomella pol ita
Loxosomella phascolosomata
Loxosomella varians
JOo" Loxosomella fauve/i
Loxosomella obesa
Loxosomella atkinsae
.~.:
Loxosomella leptoclini
~
Loxosomella v;vipara Loxosomella e/egons
Loxosoma jaegersteni Loxosoma rhodinico/a Loxosoma pectinari cola

1001'
Pedicellinc cernuc
Bcren/sic benedeni
Barenfs;c discrete Bcren/sic gracilis A Bcren/sic grccilis B Scngcvellc vine/c

FIG. 62. Drawings of all identified entoproct larvae, except those of Lo xosomella neapolitana,
L. pes and Barentsia kovalevskii, which are very poorly illustrated. All larvae, except that of Loxo-
somella obesa, are seen from the right side, and it has in some cases been necessary to reverse the
original illustrations. Loxosomella fauveli redrawn from Barrois (1877), L. obesa after Atkins
(1932a), L. phascolosomata redrawn from Cori (1936), Pedice//ina cernua redrawn from Hatschek
(1877), Barentsia benedeni redrawn from Toriumi (1944).
These considerations imply that the phylogenetic scheme which I have proposed
in an earlier paper based on the budding (Nielsen, 1964, fig. 44) must be reversed
and start with C. This was also indicated by Emschermann (1971).
If we compare the hitherto described larvae of Loxosomella (Fig. 62), it is
seen that all the larvae discussed so far are rather similar, whereas the larvae of
L. atkinsae and L. elegans are of a different type. They are very small and lack the
foot and the frontal organ. I have been unable to rear these larvae but I believe that
IS'
276 CLAUS NIELSEN
they grow and develop buds during a rather long pelagic stage; it does not seem
likely that they should later on develop a frontal organ which could enable them
to settle in the same way as the larva of L. harmeri.
The larvae of the Pedicellinidae investigated so far attach with the region just
above the retracted prototroch. The metamorphosis takes place in almost exactly
the same way as in Loxosomella harmeri, but the rotation is stronger, about 180°.
It has been observed that the protonephridia form anew from the atrial epithelium
between the mouth and the ganglion.
The larvae which lack a foot, viz., those of Barentsia gracilis A and Sangavella
vineta, may either develop a foot at a later stage or some glands producing the
secretion used at the settling may perhaps develop directly from the epithelium of
the hyposphere.
Budding
The formation of new calyces takes place in the same way in all types of ento-
procts hitherto investigated (Seeliger, 1889: Pedicellina cernua; 1890: Loxosomella
sp.; Prouho, 1891: Loxosoma annelidicola; Davenport, 1893: Urnatella gracilis;
Brien, 1957: Pedicellina cernua; Nielsen, 1966a: Loxosomella viviparaj (Fig. 63).
A thickening of the one-layered epithelium gives rise to the atrium and the whole
alimentary canal. The older authors described direct invagination of the epithe-
lium while Brien (1957) described and figured a solid proliferation of ectodermal
cells (Fig. 63 A). At the next stage a small vesicle consisting of one layer of cells lies
directly below the outer epithelium (Fig. 63 B). This vesicle becomes partially
divided by an outgrowth from the one side (Fig. 63 C), and the upper one of the
compartments thus formed differentiates into the atrium while the lower one dif-
ferentiates into the digestive tract (Fig. 63 D-F). The communication between
the atrium and the gut represents the mouth, while the anus breaks through at a
later stage. The ganglion forms as a small invagination from the bottom of the
atrium. In Urnatella gracilis the protonephridia of the calyx form through prolif-
eration from one of the epithelial cells of the atrium (Emschermann, 1965b),
and the protonephridia of the other species are probably formed in a similar way.
Scattered mesoderm cells from the parent zooid fill the space between the outer
epithelium and the gut.
In the loxosomatids, which are solitary, the buds are released from the parent
zooid. In the colonial types, the pedicellinids, a constriction of the epithelium and
the cuticle forms an incomplete septum partially separating the zooids. In many
species additional septa are formed so that the stolon consists of alternating joints
with and without calyces.
In some loxosomatids the budding takes place in a small invagination of the
parental epithelium. In species such as Loxosoma annelidicola, the larger buds
protrude from this pocket (Prouho, 1891), but in other species it appears that the
buds stay enclosed in the pocket until they are almost ready to be released (L. bocki,
oesophagus rectum
ganglion
stomach
o
A
stolon
FIG. 63. Stolon tips of Pedice/lina cernua showing the development of the buds; the relative ages
of the buds are indicated by the lettering. After Brien (1957).
Franzen, 1967). This specialization is also seen in the larvae of some species;
internal buds are thus described in the larvae of Loxosomella vivipara and Loxo-
soma jaegersteni (Nielsen, 1966a) and in some unidentified loxosomatid larvae
(Jagersten, 1964; Franzen, 1967).
SURVEY OF ECTOPROCT LIFE-CYCLES

The Ectoprocta form a very well-defined group, which by most authors is divided
into the Gymnolaemata and the Phylactolaemata. The Gymnolaemata are usually
divided into three groups: Cyclostomata, Cheilostomata and Ctenostomata
(Hyman, 1959; Brien, 1960; Prenant & Babin, 1956, 1966). Some recent authors,
however, unite the two last-mentioned groups into one, called Eurystomata (or
Cheilo-Ctenostomata) (Borg, 1926; Marcus, 1938; Silen, 1942; see also Ryland,
1970).
With regard to embryology, the Ectoprocta clearly fall into three distinct
groups: 1) Eurystomata with larval types varying between the planktotrophic
cyphonautes larvae (M embranipora, Electra, Farrella (?), Hypophorella (?)) and
lecithotrophic larvae without any trace of a gut (Scruparia, Bugula, Crypto-
sula, Walkeria), with a number of intermediate forms having a non-functional
gut or the shells of the typical cyphonautes (Alcyontdium, Flustrellidra) .. 2) Cy-
clostomata which through polyembryony form almost radially symmetrical larvae
devoid of any gut; and 3) Phylactolaemata where the larvae already before the
278 CLAUS NIELSEN
liberation from the mother zooid have formed one to several polypides, and whose
"larvae", thus, must be regarded as young free-swimming colonies.
The following three sections aim at summarizing the known data on life-cycles
of the Ectoprocta in order to facilitate some phylogenetic considerations.
E UR YSTOMATA
Embryology
Among the eurystomes the fertilization has only been witnessed by Silen (1966),
who made his observations on two species of Electra. He found that the spermato-
zoa are released through the tips of the pair of adneural tentacles, drift through
the water and are caught by the tentacles of other zooids. In E. posidoniae they
attach to the outer unciliated surfaces of the tentacles and stay motionless until an
egg is about to emerge through the intertentacular organ. Then the spermatozoa
become mobile and approach the egg; the spermatozoan's penetration of the egg
was not observed.
There are indications that this type of fertilization, with slight modifications,
occurs in other eurystomes. Marcus (1926a) observed spermatozoa adhering to
the tentacle crown of Farrella, Strom (1969) observed the same phenomenon in
Triticella, and Bullivant (1967) observed the release of spermatozoa through the
pair of adneural tentacles in Schizoporella and Zoobotryon. Silen (1966) observed
that spermatozoa gathered in the intertentacular organ of zooids of Electra cru-
stulenta and disappeared when an egg was shed.
It seems probable that cross-fertilization takes place in the same way in all
eurystomes, but further investigations are desirable.
Some cheilostome species shed their small eggs directly into the water, where
they develop into the well-known shelled cyphonautes larvae (Membranipora,
Conopeum, Electra; see Table 1). A similar type of development occurs in certain
ctenostome species (Alcyonidium albidum, Farrella, Hypophorella; see Table 1),
but none of these larvae have been observed in the fully developed stage, and it is
not directly known if they are planktotrophic. Ehlers (1876) has observed some
shell-like formations, which he believed might be shells of the metamorphosed
larva of Hypophorella expansa, but it is not certain whether shells develop at all in
these larvae.
Most of the eurystomes, however, protect the embryos in some way; an excel-
lent survey of the various types of brood protection is given by Hyman (1959,
pp 331-339).
Some lecithotrophic larvae have shells (Flustrellidra, Pherusella) and some
develop a non-functional gut (Alcyonidium polyoum; see Table 1).
It appears from the literature (Table 1) that early development of all species
follows one and the same pattern and that all types of transitions exist between the
(continued page 282)
TABLE 1. A key to the literature on embryology and larval types of the Eurysto-
mata. Papers describing the larvae in so vague terms that the larval type cannot be
distinguished have generally been omitted. The nomenclature follows Prenant &
Bobin (1956, 1966) or Bassler (1953). The larval type is indicated as follows: s, the
larva has a pair of shells; n, the larva is naked; p, the larva is planktotrophic; 1, the
larva is lecithotrophic. The parts of the life-cycle described in each paper are in-
dicated in parantheses: e, embryology; 1, larva; m, metamorphosis.
* Full synonomies and reference lists for the cyphonautes larvae of Membranipora
membranacea and Electra pilosa are given in Ryland (1964).
CTENOSTOMATA
CARNOSA
HALCYONELLOIDA
s - 1 Flustrellidra hispida (as Flustrella h.): Hincks (1851: 1, m), Redfern (1858: 1, m),
Barrois (1877: e, 1, m), Prouho (1890: 1, m; 1892: m), Pace (1906: e, 1); (as
Alcyonidium h.): Joliet (1877: 1, m).
s -1 Pherusella tubulosa (as Pherusa t.): Prouho (1892: 1, m).
s -I? P. brevituba: Soule (1953: m).
n -1 Alcyonidiumpolyoum + A. mytili: Barrois (1877: e, 1, m), Harmer (1887: e, 1),
Prouho (1892: e,l, rn), Seeliger (1906: 1), Zschiesche (1909: m); (as Sarcochitum
polyoum): Joliet (1877: 1, m).
n -1 A. variegatum: Prouho (1892: 1).
n -1 A. duplex: Prouho (1892: 1).
n -1 A. hirsutum: Ryland (1962: m); (as Cycloumpapillosum): Hincks (1851: 1).
s? - p? A. albidum: Prouho (1892: e, 1).
n -1 A.gelatinosum: Barrois (1875: e, 1); (as Halodactylus diaphanus): Farre (1837: 1).
PALUDICELLOIDA
n -1 Nolella dilatata (as Cylindroecium d.): Prouho (1892: e).

n -1 N. gigantea: Marcus (1939: 1).
n -1 N. papuensis: Silen (1944a: e).
n -1 Victorella pavida: Toriumi (1944: 1, m).
n -1 V. muelleri (as Paludicella (Tanganella) m.): Braem (1951: e, 1, m).
n -1 Sundanella sibogae (as Victorella s.): Braem (1939: e, 1).
n -1 Paludicella articulata (as P. ehrenbergi): Braem (1896: e, 1).
n -1 Bulbella abscondita: Braem (1951: e, 1, m).
STOLONIFERA
WALKEROIDA
n -1 Walkeria uva (as Vesicularia cuscuta): Barrois (1877: e, 1, m), Joliet (1877: e, 1);
(as Bowerbankia, see Ostroumoff, 1886, p. 188): Repiachoff (1880: e, 1); (as
Vesicularia uva): Ostroumoff (1886: m).
n? - p? Farrella repens: Marcus (1926a: E' 1).
n? - I? Triticella koreni: Strom (1969: e, 1).
s? - p? Hypophorella expansa: EWers (1876: e, 1), Prouho (1892: e, 1).
280 CLAUS NIELSEN
VESICULARIOIDA
n -1 Amathia lendigera: Ca1vet (1900: 1); (as Serialaria 1.): Barrois (1877: 1, 1886:
e, 1, m).
n -1 A. semiconvoluta: Calvet (1900: e, 1).
n -1 Zoobotryon verticillatum: Zirpolo (1933: I, m).
n -1 Bowerbankia imbricata: Joliet (1877: 1).
n - 1? B. stationis (as Vesicularia .1'.): Ostroumoff (1886: 1, m).
n -1 B. pustulosa: Ca1vet (1900: e, 1).
CHEILOSTOMATA
ANASCA
SCRUPARIOIDA
n - 1 Scruparia sp. (as Eucratea chelata): Barrois (1877: 1).
MALACOSTEGOIDA
s - p Membranipora membranacea" (Cyphonautes schneideri, C. borealis): Atkins

(1955a: 1, m; 1955b: 1), Ryland (1964: 1; 1965a: 1).
s - P M. denticulata: Ostroumoff (l885a: 1; 1886: 1).
s - P M. tuberculata (Cyphonautes sargassi?): Lohman (1904: 1); (as Nichtina t.):
Hastings (1930: m).
s - p M. villosa (Cyphonautes occidentalis): Robertson (1908: 1, m), O'Donoghue
(1926: 1, rn).
s - p Conopeum reticulum: Cook (1964: 1, m), Ryland (l965a: 1).
s - P c. seurati: Cook (1962: e; 1964: 1, m), Ryland (1965a: 1), Cook & Hayward
(1966: e, 1, m).
s - p Electra pilosa* (Cyphonautes compressus, C. balticus): Atkins (l955a: 1, m;
1955b: 1), Ryland (1964: 1; 1965a: 1); (as Membranipora p.y: Schneider (1869:
1, m), Prouho (1892: e, 1), Kupelwiser (1905: 1, m), Cori (1941 : 1).
s - P E. monostachys: Cook (1964: 1), Ryland (1965a: 1).
s - P E. erustulenta (Cyphonautes barroisi): Lohman (1911: 1), Levander (1913: 1),
Cook (1961: 1, m; 1962: e, 1), Ryland (1965a: 1).
s - p? E. angulata: Mawatari (1953: 1).
s - P E. posidoniae: Ranzoli (1963: 1, m).
n -1 Tendra zostericola: Nordmann (1840: 1, m), Repiachoff (1875a: 1, m; 1878b:
e; 1879: e; 1880: e, 1); (as Membranipora z.): Ostroumoff(l886: 1, m), Braiko
(1967: 1, m).
s - p T. repiachowi (as Membranipora r.): Ostroumoff(1885a: 1886: 1).
n -1 Flustra [oliacea: Barrois (1877: e).
n ? -I? Carbasea carbasea (as Flustra c.): Grant (1827: 1, m), Stach (1938: e).
n? -1? C. indivisa: Stach (1938: e).
n? -1? Securiflustra securifrons (as Flustra .1'.): Cal vet (1900: e).
n -1 Callapara dumerili: Silen (1944b: 1).
n -1 Crassimarginatella leucocypha: Marcus (1939: 1).
n -1 Amphibiestrum fiemingi (as Membranipora f.i: Calvet (1900: e, 1).
COELOSTEGOIDA
n -1 Thalamoporella evelinae: Marcus (1939: 1; 1941a: e).
PSEUDOSTEGOIDA
n -1 Cellaria salicomia (as C. fistulosa): Ca1vet (1900: e, 1, m).

n -1 C. salicornioides: Calvet (1900: e, 1, m).
CELLULARIOIDA
n -1 Scrupocellaria scruposa: Nitsche (1869: 1), Barrois (1877: e, 1), Ca1vet (1900:
e,l).
n -1 S. bertholleti (as Cellaria capreolusy: Ostroumoff (1886: 1).
n -- 1 S. reptans: Ca1vet (1900: e); (as Canda 1'.): Barrois (1877: e, 1).
n -1 Tricellaria occidentalis: Mawatari (1951b: e, 1, m).
n -1 Caberea boryi: Ca1vet (1900: e).
n -1 Synnotum aegyptiacum: Marcus (1941b: e).
n -1 Bicellariella ciliata: Nitsche (1869: 1), Barrois (1877:1).
n -1 Bugula neritina: Ca1vet (1900: e, 1, m), Mawatari (1946a; 1, m; 1946b: 1; 1951a:
e, 1, m), Lynch (1947: 1, m), Ryland (1960: 1), Wisely (1963: 1, m); Woolla-
cott & Zimmer (1971: 1, m),
n -1 B. calathus: Vigelius (1886: e, 1, m; 1888: m), Ca1vet (1900: e, 1).
n -1 B.flabellata: Nitsche (1869: 1, m), Barrois (1877: 1, m; 1886: 1, m), Correa (1948:
e, 1), Ryland (1960: 1).
n -1 B. simplex: Lynch (1960: 1), Ryland (1960: 1); (as B. sabatieri): Ca1vet (1900:
e, 1, m); (as B. flabellata): Grave (I 930: 1, m),
n -1 B.fulva: Ryland (1960: 1); (as B. ditrupae): Marcus (1938: 1).
n -1 B. turbinata: Ca1vet (1900: e, 1), Ryland (1960: 1).
n -1 B. plumosa: Nitsche (1869: 1), Sa1ensky (1874: 1), Barrois (1877: 1).
n -1 B. gracilis (as B. turrita): Marcus (1938: 1), Lynch (1949: 1; 1960: 1).
n -1 B. avicularia: Marcus (1938: e, 1).
n -1 B. stolonifera: Ryland (1960: 1); (as B. aviculariay: Ca1vet (1900: e, 1, m).
n -1 B. californica? (see Zoological Record, Bryozoa, 1951): Mawatari (1946c: 1, m).
n -1 Caulibugula mortenseni (as Stirpariella m.): Marcus (1926c: e).
CRIBRIMORPHA
n - 1 Membraniporella nitida (as Membranipora n.): Barrois (1877: 1).
ASCOPHORA
n -1 Hippothoa hyalina (as Mollia h.): Barrois (1877: 1, m).
n -1 Haplopoma impressum (as Mollia gran!fera): Barrois (1877: 1).
n -1 Hippopodina [eegeensis: Marcus (1938: e).
n -1 Chorizopora brongniarti: Ca1vet (1900: e, 1).
n -1 Schizobrachiella sanguinea (as Schizoporella s.): Ca1vet (1900: e, 1).
n -1 Schizoporella unicorn is (as Lepralia u.): Barrois (1877: 1; 1879/80: e, 1, m).
n -1 S. carvalhoi: Marcus (1939: 1).
282 CLAUS NIELSEN
n -1 Escharina vulgaris (as Lepralia ciliata): Barrois (1877: 1, m).

n -1 E. spinifera (as Lepralia s.): Barrois (1877: e, 1, m).
n -1 Hippodiplosia americana: Marcus (1938: 1).
n -1 Hippoporellagorgonensis: Marcus (1939: 1).
n -1 Escharoides coccineus (as Lepralia c.): Gosse (1853: 1, m), (as Discopora c.):
Barrois (1877: e, 1).
n -1 Microporella ciliata: Calvet (1900: e), Marcus (1938: e, 1).
n -1 Fenestrulina malusi (as Microporella m.): Pergens (1889: e, 1, m).
n -1 Porella concinna: Barrois (1877: 1).
n -1 Smittina collifera: Mawatari (1946d: m).
n -1 Rhynchozoon phrynoglossum: Marcus (1938: e, 1).
n ~I Cryptosula pallasiana (as Lepralia p.): Smitt (1865: 1), Repiachoff (1875b: e, 1,
m; 1878a: e), Barrois (1877: 1, m; 1886: 1, m), Ostroumoff(1886: 1, m), Calvet

(1900: e, 1, m).
n -1 Watersipora cucullata: Marcus (1938: 1), Mawatari (1952: e, 1), Wisely(1958:1, m).
n -1 Cellepora pumicosa: Barrois (1877: 1).
n -1 Hippothoa hyalina (as Celleporella h.): Ryland (1962: 1).
n -1 Costazia costazi (as Siniopelta c.): Marcus (1938: e).
n -1 Holoporella mordax: Marcus (1938: e, 1).
n -1 Catenicella contei: Marcus (1939: 1).
n -1 Savignyella lafonti: Marcus (1939: 1).
cyphonautes larvae and the lecithotrophic larvae devoid of any trace of a gut
(Victorella, Amathia, Bugula). For comparative purposes it must, therefore, suf-
fice to summarize the development of a few species.
The larva of Electra pilosa is the cyphonautes larva which has been most
thoroughly studied (Table 1), and the only one in which the metamorphosis has
been studied on sections (Kupelwieser, 1905). As will be seen from the following
summary, several stages of the development are still in need of a more detailed
study.
The early development has been studied by Prouho (1892). The cleavage is
total and equal, and the 16-cell stage (Fig. 64A) is biradial with an upper and a
lower oval tier consisting of eight cells each. There is a small blastocoele at this
stage and the cells of each tier are arranged in two only slightly curved lines. The
32-cell stage (Fig. 64B) consists of two cell layers each comprising 4 X 4 cells;
the vegetative layer is flattened and its four central cells are more rich in yolk than
the others. These four cells are said to represent the entoderm, which is probably
formed through invagination (Fig. 64 C); the blastopore closes soon after the
gastrulation. It is not clear whether Prouho (1892) has seen the mesoderm cells in
this species, but in Alcyonidium albidum he observed a pair of small mesoderm
cells "one on each side of the plane of symmetry"; these cells are stated to lie in
the anterior end of the embryo.
During the following phase the number of cells grows considerably and the
283
..•
ENTOPROCT LIFE-CYCLES
~ : -'" _~I:
:._."~ -t
.
- - - - ., - ':.-- .
," -,,~ ~
A o 51
IOO~
E
FIG. 64. Early development of Electra pilosa. A, 16-cell stage in oblique view; B, 32-cell stage seen
from below; C, an optical section of a young gastrula; D, an optical section of a young larva in
which the stomodaeum has just formed; E, an optical section of a young larva showing the procto-
dae1 invagination; F, an optical section of an almost fully developed larva showing the invagina-
tion to form the adhesive sac. Redrawn from Prouho (1892). as, adhesive sac; me, mesodermal
cells in front of the stomodaeum; pr, proctodaeum; st, stomodaeum.
apical organ starts to differentiate at the animal pole. Next, the embryo becomes
more conical and a wide invagination appears on the lower side. The egg mem-
brane comes into close contact with the apical organ and the lower side of the
embryo and it soon seems to disappear in these regions. At the same time cilia
begin to develop at the apical organ and at the corona cells around the lower in-
vagination. The larva is now able to swim. The mesoderm cells start to multiply,
and some of them become arranged in a row between the anterior part of the coro-
na and the apical organ. The mass of entoderm cells becomes hollow and a com-
munication forms between this cavity and the bottom of a conical invagination
of the lower side of the larva, thus forming the stomodaeum (Fig. 64 D). The
larva now becomes markedly compressed laterally. The proctodaeum forms as
a small invagination from the posterior end of the large ventral invagination
(Fig. 64E). Cilia develop on the upper part of the large invagination and the larva
begins to feed.
A pair of ciliated knobs develops from the epithelium at about the middle of
the corona, and between these a ciliated ridge forms, passing just in front of the
anus; this ridge separates the anterior inhalant chamber from the posterior ex-
halant chamber. Another pair of ciliated knobs develops on the corona between
the already mentioned pair and the anterior side of the corona, and a pair of cili-
ated thickenings forms from these knobs and runs anteriorly inside the anterior
part of the corona. The middle parts of the corona between the two pairs of knobs
become less heavily ciliated.
284 CLAUS NIELSEN
apicaI 0 rg an -----,~~4:':rrTI" oesophagus
oesophagus constrictor
adhesive
corona
ciliated thickening
exhalant chamber
ciliated ridge velum inhalant chamber
FIG. 65. Left half of a fully grown larva of Electra pilosa seen from the right. Schema based on
Prouho (1892), Kupelwieser (1905) and Atkins (1955b).
At a somewhat later stage the adhesive sac forms as a small invagination of the
epithelium just in front of the anus (Fig. 64 F). The invaginated epithelium thick-
ens and the whole organ becomes quite voluminous, with a pair of forward-directed
lateral expansions. The pyriform organ apparently forms through a thickening
of an invagination of the epithelium between the anterior ciliated thickenings. The
whole organ becomes ciliated, and a tuft of especially long cilia, the vibratile
plume, develops at the front end of the organ.
The velum, which was apparently overlooked by Prouho (1892), is aU-shaped
fold of the lower side of the epithelium of the inhalant chamber; it follows the pos-
terior side of the pyriform organ, and its two sides run to the ciliated ridges. The
velum carries a row of cilia and has a constrictor muscle which continues through
the upper part of the ciliated ridge.
Finally, the lateral sides of the larva become covered with a pair of chitinous
shells which can. be closed through contraction of a large and a small adductor
muscle situated in front of the adhesive sac.
The fully developed cyphonautes larva (Figs 65-66) is described by Prouho
200 ~
FIG. 66. An optical section of a fully grown larva of Electra pilosa, showing the most important
nerves and muscles; the nerves are dotted, the smooth muscles fully drawn and the striated muscles
dashed. Schema based on Prouho (1892) and Kupelwieser (1905). Compare with Fig. 65.
(1892), Kupelwieser (1905) and Atkins (1955b). The apical organ has a tuft of stiff
cilia, and small cilia, probably of sensory function, occur at the anterior and pos-
terior edges of the larva, between the shells. Kupelwieser (op. cit., pp 19-24) de-
scribes the morphology of the ciliated cells in detail, but unfortunately it is not
known how the various rows of ciliated cells of the corona, the ciliated ridges and
the velum are connected. The function of the ciliary apparatus in feeding is described
by Atkins (1955b).
The muscles of the larva (Fig. 66) are of two types. A pair of bundles of
smooth fibres runs from the shells near the middle of the anterior edge to the dor-
sal side of the adhesive sac, where the fibres spread between the cells. The adductor
muscles mentioned above are also smooth. Striated retractors originate at the shells
and insert on the cells of the corona. A double bundle of striated fibres follows the
dorsal edge of the larva, and a pair of the fibres enters the apical organ. At the
anterior side a few fibres enter the pyriform organ and run forward to the base of
the vibratile plume while other fibres spread over the surface of the pyriform organ
286 CLAUS NIELSEN
and the ciliated thickenings. At the posterior side the bundles split up and attach
to the posterior part of the corona. Other important striated muscles are the
constrictors of the ciliated funnel, one fibre following the base of the corona cells
and the above-mentioned constrictor muscle of the velum.
The nervous system (Fig. 66) is not known in detail, but the main nerves have
been described by Prouho (1892) and Kupelwieser (1905). A pair of nervesfollows
the muscles from the pyriform organ to the apical organ, where most of the fibres
enter between the cells. A few fibres follow the muscles backwards along the poste-
rior edge to the corona, and one nerve possibly follows the coiled muscle to its
insertion at the shell. At the pyriform organ the nerves split into a median branch,
which enters the organ and runs to the cells of the plumet, and a lateral branch. A
nerve splits off from this branch and innervates the ciliated lateral thickenings of
the pyriform organ, while the other part of the nerve continues to the corona where
it splits into an anterior and a posterior branch which follow the basis of the outer
row of ciliated cells of the corona. A small nerve branches off from the corona
nerve and follows the ciliated ridge.
Schneider (1869) followed the metamorphosis of a cyphonautes larva and
found that the ancestrula belonged to Electra pilosa. Also Barrois (1877) and At-
kins (1955 a) have followed the metamorphosis. A detailed description of the
metamorphosis and the formation of the polypide bud has been given by Kupel-
wieser (1905). When the larva is ready to settle it starts to creep with the protruded
pyriform organ sliding along the substratum. When a suitable spot has been selec-
ted the larva contracts all the striated muscles strongly, whereby the soft parts
become rather spherical, the adductor muscles are torn apart and the shells open.
According to Kupelwieser (op. cit.), the shells are connected at the anterior angle
and behind the apical organ so that the antero-dorsal parts of the shells come to
overlap when the shells open widely. The adhesive sac evaginates and spreads over
the substratum as a thin plate, and the smooth muscles between the shells and the
dorsal side of the adhesive sac contract strongly, pulling the shells against the
substratum (Kupelwieser, 1905, fig. 24). The newly settled larva is thus quite flat
(Fig. 67 A). The edge of the everted adhesive sac is somewhat thickened and comes
into contact with a ring of gland-like cells just above the corona. The one-layered
epithelium of the episphere and the adhesive sac thus lines the young ancestrula,
which is still for some time covered by the larval shells. Soon after the settling all
larval organs start to disintegrate and only the apical organ, which has become
retracted so as to form a small invaginated sac, persists (Fig. 67 B).
The invaginated apical organ forms the polypide bud, which grows rapidly and
becomes two-layered (Fig. 67 C). It seems very peculiar that the polypide bud forms
from the apical organ of the larva. In species of Membranipora twin ancestrulae
develop (see, e. g., Atkins, 1"955 a) and here the two polypide buds probably origi-
nate frqm the epithelium of the episphere, independently of the apical organ.
Some of the more specialized cell types of the larva, such as muscle cells and
aD De
A
ip op
FIG. 67. Settling and formation of the polypide bud in Electra pilosa, median sections. A, a newly
settled larva, the various larval organs can still be recognized; B, the apical organ is fully invagi-
nated and the other larval organs are degenerating; C, the polypide bud has two distinct layers,
only fragments of some of the larval organs can be recognized. A, C from Kupelwieser (1905)
after Brien (1960), B redrawn from Kupelwieser (1905). ao, apical organ; as, adhesive sac; co,
corona; de, degenerating ciliated cell; dm, degenerating muscle cell; ip, inner layer of the po-
lypide bud; mu, muscles between the pyriform organ and the posterior part of the corona; oe,
oesophagus; op, outer layer of the polypide bud ~ po, pyriform organ; sh, shell; st, stomach;
vp, vibratile plume.
the cells of the corona, with the strong ciliary rootlets, can during the development
of the polypide still be recognized among the histolyzing cells.
The following stages of development of the polypide have not been investi-
gated, but it can be seen from the drawings of Kupelwieser (1905) and Atkins
(1955a) that the orifice of the ancestrula develops in the posterior end of the larval
body, i. e., the retracted tentacles of the ancestrula point posteriorly with respect
to the orientation of the cyphonautes larva.
In all the eurystomes which have brood protection the larvae are liberated from
the colony when they are almost ready to metamorphose; their planktonic life is
short, probably only few hours in most cases.
288
L
CLAUS NIELSEN
Cs
ig
500
re
~
M
D
The lecithotrophic larvae which resemble the cyphonautes larvae most closely
are those of Flustrellidra and Pherusella, which have a pair of shells (Table 1).
The first cleavages of Flustrellidra hispida (Fig. 68) follow much the same pat-
tern as that described above for Electra pilosa (Pace, 1906). The 32-cell stage con-
sists of 16 smaller animal cells arranged in two tiers and 12 medium-sized cells
surrounding four large vegetative cells. This pattern seems to be characteristic of
practically all eurystomes. (The drawings of whole embryos and of sections by
Pace (op. cit.) are not always quite in accordance with respect to the shape of the
embryos; the sections show regularly rounded embryos while the whole embryos
have more irregular outlines and appear to have been pressed during handling. I
have therefore redrawn the embryos with more rounded outlines.)
Next, the four large vegetative cells divide horizontally (Fig. 68 D), and shortly
afterwards the four lower cells move into the blastocoele (Fig. 68 E). These eight
internal cells form a compact mass in which the cells divide, but it is not at any
stage possible to distinguish ento- and mesoderm cells. During the following
development the animal cells can be recognized as being somewhat flattened while
the vegetative cells are rather high (Fig. 68 F). Barrois (1877) stated that the twelve
cells surrounding the four large vegetative cells can be followed through these
stages and that they become the cells of the corona. According to Pace (1906) the
corona and the whole epithelium of the hyposphere derive from these twelve cells.
The adhesive sac forms as a median invagination from the lower side of the
embryo and in front of this a stomodaeal invagination soon appears (Fig. 68 G).
The stomodaeum does not communicate with a stomach at any stage, and Pace
(1906) believed that it possessed a glandular function, which is also suggested by
the general appearance of the cells. Somewhat later the pyriform organ develops as
a depressed area of thickened ectoderm. The apical organ and the (?) unpaired
neuro-muscular strand connecting it with the pyriform organ likewise develop at
this stage.
The embryo becomes laterally compressed and cilia develop on the cells just
FIG. 68. The development of Flustrellidra hispida. A, 16-cell stage seen from above and below; B,
20-cell stage seen from above and below; C, 32-cell stage seen from above and below, and in me-
dian section; D, a median section, the four vegetative cells have divided horizontally; E, a me-
dian section of a gastrula which has almost closed the blastopore; F, a vertical section of an em-
bryo, showing the low epithelium of the episphere, the high epithelium of the hyposphere and the
mesendodermic mass; G, a median section of an older embryo with stomodaeum, pyriform organ
and adhesive sac; H, a median section of a fully grown larva; I, a median section of a newly
settled larva; K, a transverse section of a rather newly settled larva, showing the invagination
forming the polypide bud; L, a reconstruction of a median section of a young polypide; M, a
median section of a young ancestrula. A-H redrawn from Pace (1906), I-M redrawn from Prouho
(I 890). ao, apical organ; as, adhesive sac; ig, invagination to form the ganglion; mo, mouth; po,
'pyriform organ; re, rectum; rrn, retractor muscles; sh, shell; si, stomodaeal invagination; st,
stomach; ve, vestibule.
19
290 CLAUS NIELSEN
below the groove separating the flattened animal cells from the ventral ectoderm.
At this stage the chitinous shells covering the whole hyposphere except the apical
organ develop, and a narrow cavity forms in the mesentodermic mass (Fig. 68 H).
Pace (1906) regards this cavity as the cavity of the stomach.
The internal sac becomes strongly thickened and the "stomach" and pharynx
degenerate and leave only a rather loose layer of cells, some of which have been
described as mesoderm by Prouho (1890).
Prouho (1890) has described the fully developed larva, which resembles a very
elongated cyphonautes larva without a gut. The apical and pyriform organs
consist of the same cell types as those of the cyphonautes larva and they are con-
nected with an (?) unpaired neuro-muscular strand whose nerve fibres can be fol-
lowed to the cells of the vibratile plume, the ciliated lateral thickenings of the py-
riform organ and the corona. The muscular system comprises a small adductor
muscle, a ring muscle following the base of the corona, lateral muscles originating
on the shells and inserting on various parts of the epithelium of the hyposphere,
and a pair of lateral longitudinal muscles. The adhesive sac is large and elongated
and fills most of the body cavity of the larva. The corona consists of a single row
of heavily ciliated cells showing strong ciliary rootlets. Some of the epithelial
cells of the narrow hyposphere carry small ciliated knobs resembling those of the
lower part of the inhalant chamber of the cyphonautes larva. Braem (1951, p. 41)
describes a small proctodaeal invagination which does not communicate with the
stomach.
After a short pelagic life, the larva settles by everting the adhesive sac in
contact with the substratum (Prouho, 1890). At the same time, most of the muscles
contract strongly and the soft parts of the larva loosen from the shells. The
thickened edge of the everted adhesive sac unites with the cells just above the
corona, and just as in Electra pilosa, the whole corona and the pyriform organ
become enclosed in a ring-shaped cavity (Fig. 68 I). The apical organ retracts into
a small invagination and the thickened ectoderm along the mid-dorsal line of the
larva closes above it. The muscles originating at the posterior parts of the valves
and running to the thickened dorsal ectoderm are said to persist as the parietal
muscles of the ancestrula (Prouho, 1890, p. 437).
The larval organs degenerate and a thin cuticle becomes secreted over the
young ancestrula; the larval valves lie loose on top of the ancestrula during most
of the following development. Prouho (1890) describes a distinct cell plate below
the central part of the thickened dorsal epithelium in the area of the apical organ.
This central area of the young ancestrula, the "meso-ectodermal disc", can be
observed on live specimens as a faint transparent area; the polypide develops from
this area. According to Prouho (op. cit.) the two layers form one invagination, but
his drawing (Fig. 68 K) shows two areas in the invagination, and they are perhaps
comparable to the rudiments of the vestibule (formed from the ectoderm) and the
polypide bud (formed from an inner layer of cells) of the cyclostomes (Nielsen,
~
. o
o 0
o 0
o 0
A,
8, 82
c E
D,
50jJ
FIG. 69. Embryology of Bugula flabellata. A, 16-cell stage seen from above; B, 32-cell stage seen
from above and below; C, median section of a 60-cell stage; D, 64-cell stage seen from above and
below; E, median section of a 64-cell stage; F, median section of an embryo, showing the primor-
dia of the apical organ, the pyriform organ and the adhesive sac. The corona cells are dotted in
C, E and G and in one of the quadrants in Band D. Redrawn from Correa (1948). ao, apical organ;
as, adhesive sac; po, pyriform organ.
1970). It appears that Prouho (1890) has only made transverse sections of the de-
veloping polypide, which makes it rather difficult to follow his description of the
formation of the various parts of the polypide. His reconstruction of a median
section (Fig. 68 L) shows a two-layered sac from which a small protrusion develops
on the lower side. This protrusion is described as the rectum, and the intestine
should be formed from a mass of cells just in front of the rectum. A pharynx de-
velops from the opposite end of the sac and a communication finally forms between
the bottom of the pharynx and the stomach/intestine. The tentacles develop as
thickenings of the epithelium around the mouth and the ganglion forms as a small
invagination of the ectoderm at the base of the tentacles near the pharynx (Fig.
68 M). The contracted tentacles of the ancestrula point towards the posterior part
of the larval body.
19·
292 CLAUS NIELSEN
Alcyonidium polyoum + A. mytili has a larva which lacks the shells and de-
velops a rudimentary stomach which connects with the stomodaeal invagination,
but the stomach degenerates before the larva is liberated (Barrois, 1877; Harmer,
1887). Its metamorphosis and the following formation of the first polypide has
been followed by Zschiesche (1909), but although his descriptions and the accom-
panying drawings are rather detailed, it is not clear how the various cell layers
develop, and also this description lacks drawings of longitudinal sections of the
early stages of the developing polypide.
However, most of the eurystome larvae which have been described hitherto
lack any trace of a gut (Walkeria, Bowerbankia, Scruparia, Amphiblestrum, Tha-
lamoporella, and all species belonging to the groups Paludicelloida, Pseudostegoida,
Cellularioida, Cribimorpha, and Ascophora, see Table 1).

The development of Bugula can be taken as representative of this type. Larvae
of several species of this genus have been described, and they only seem to differ
from each other in small details, such as the number and arrangement of the red
or black pigment spots usually interpreted as eye-spots.
The cleavage of B. ftabellata (Fig. 69) has been described by Correa (1948).
The pattern is much the same as that described above for Electra and Flustrellidra.
In species of genera such as Hippothoa and Holoporella, which have ellipsoidal
eggs, it has been observed that the first cleavage is transverse and divides the egg
into an anterior and a posterior half (Marcus, 1938, p. 93). The animal and vege-
tative tiers of the 8-cell stage consist of cells of equal size. By the 64-cell stage four
internal cells have been deliminated at the vegetal pole (Fig. 69 E) and formed
the entoderm, which at a somewhat later stage arranges as a small archenteron
(Fig. 69 F).
The 16 cells of the third tier divide once more and Correa (1948) states that
these 32 cells grow enormously to form the corona, which covers most of the sur-
face of the larva (Fig. 70 A-B). Woollacott & Zimmer (1971) state, however, that
the corona consists of a ring of about 230 cells, and similar high numbers are also
shown by horizontal sections of other larvae (see e.g., Calvet, 1900, pl. 12, fig. 2).
Cilia develop on the corona cells at an early stage. The epithelium of the apical
area thickens and forms the apical organ, which becomes connected with the de-
veloping pyriform organ by a neuro-muscular strand. The glandular area above
the ciliated groove with the vibratile plume can soon be recognized in the develop-
ing pyriform organ. Calvet (1900, p. 360) states that the nervous connection
between the apical and pyriform organs is paired in B. simplex and that each lateral
nerve sends fibres to the cells of the vibratile plume, the cells of the ciliated groove
and the corona cells, just as in the cyphonautes larva.
Finally, the adhesive sac develops as an invagination of a thickened, one-
layered epithelial area behind the pyriform organ.
The adult larva of B. neritina and its metamorphosis have been described by
Calvet (1900) and in detail by Woollacott & Zimmer (1971); also Lynch (1947)
vibratile plume apical organ sensory cap of the apical organ
cilia
superior glandular
field of the
pyriform organ
neuro-
muscular
strand
syncilium of
the vibratile
plume ring muscle
A
B
"roof" of the adhesive sac
ciliated groove "neck"

of the pyriform organ
"wall"
200~
----- -----
C D
FIG. 70. The larva and metamorphosis of Bugula neritina. A, a free-swimming larva in antero-
lateral view; B, schema of a median section of a larva; CoD, schemata of vertical sections of two
stages of the metamorphosis of the larva. A redrawn from Calvet (1900) (not exactly to scale),
B-D redrawn from Woollacott & Zimmer (1971).
and Mawatari (1951 a) described the major features of the settling. The larva (Fig.
70A-B) is ovoid and is covered by the heavily ciliated corona cells except at the
upper and lower poles, and at the frontal side where the elongated pyriform organ
with a group of gland cells, the vibratile plume and the ciliated groove, makes a
narrow interruption. Longitudinal bands of small pigmented cells are found be-
tween the corona cells but they do not reach the surface of the larva. Two large
longitudinally elongated pigment spots, in the centres of which are narrow pits
with a tuft of cilia, occur at the latero-posterior part of the larva; they lie close to
the corona ring-nerve and are usually interpreted as eye-spots. Above the corona
occurs a ring of cells with spherical protrusions and above this is found a ring-
shaped infolding with a somewhat thickened epithelium at the bottom (the "pal-
lial" epithelium). The peripheral part of the apical organ consists of a wide torus
of columnar epithelium having a characteristic embryonal appearance with "a
wealth of free ribosomes" (Woollacott & Zimmer, 1971, p. 356) and large nuclei
294 CLAUS NIELSEN
with conspicuous nucleoli. A tissue of similar shape and appearance lies directly
beneath this torus. Woollacott & Zimmer (1971) call these two layers "upper and
lower blastemas". The center of the apical organ is occupied by a small, kidney-
shaped cell plug without cilia; basally it continues into a neuro-muscular strand
sending branches to the roof of the adhesive sac, the pigmented spots, the vibratile
plume and a circular band level with the nuclei of the corona cells. The central
cell plug is surrounded by a collar of ciliated cells which extend in narrow rays
over the apical area; these rays of ciliated cells lie on rays of pigmented cells (Fig.
70B). Below the corona cells is another ring of cells with spherical protrusions
and a ring of sparsely ciliated cells surrounding the opening of the adhesive sac.
This voluminous organ shows three regions, the "neck" region, the "wall" region
and the "roof" region.

The markedly photopositive larva has a planktonic stage which lasts less than
12 hours. It soon starts creeping with the ciliated groove and the vibratile plume
pressed against the substratum (Mawatari, 1951a, fig. 4A), and the larva now and
then changes its shape through strong irregular muscle contractions. At the begin-
ning of the metamorphosis the adhesive sac suddenly everts (Fig. 70C) and its
"roof" region spreads over the substratum. The lower part of the corona cells and
the "neck" region of the adhesive sac have by this process become infolded in a
deep equatorial furrow, whereas the furrow around the apical organ has become
widened.
Next, the large circular fold of the "wall" region of the adhesive sac unfolds and
stretches along the upper part of the corona cells to reach the peripheral part of
the "pallial" epithelium (Fig. 70D). The whole apical region has now become
retracted so as to form a depression in the center of the larva, surrounded by the
now very high "pallial" epithelium. Finally, the central part of the apical area
becomes further retracted so that the lower blastema comes to surround the upper
blastema, which in turn surrounds the ciliated and pigmented cells of the apical
organ, while the upper edge of the adhesive sac constricts above (Fig. 70D). The
epithelium of the adhesive sac now covers all sides of the metamorphosed larva;
this is in contrast to what has been described in the metamorphosis of Electra
(p. 286), Flustrellidra (p. 290) and Alcyonidium (Zschiesche, 1909), but a similar
total enclosure by the adhesive sac has been observed in Scrupocellaria by Braem
(1951, p. 29).
The whole surface of the young ancestrula now becomes covered by a thin
cuticle and the larval organs start to degenerate except for the two blastemal
layers. These two cell layers give rise to the polypide bud, the upper blastema dif-
ferentiating into the ecto- and entoderm of the polypide and the lower blastema
forming the "mesodermal" lining of the polypide. The "mesodermal" lining of the
cystid is by Woollacott & Zimmer (1971) believed to originate from the pigmented
cells between the basal parts of the corona cells. The details of the polypide de-
velopment remain unknown.
co
as "rno"
100p
ao
FIG. 71. A, a median section of a large embryo of Victorella muelleri; B, a median section of a
larva of Victorella muelleri; C, a median section of a newly settled larva of Victorella muelleri;
D, a median section of a settling larva of Bulbella abscondita. The asterisks indicate the region
just above the corona. Redrawn from Braem (1951). ao, apical organ; as, adhesive sac; co,
corona; po, pyriform organ.
Small deviations from the general pattern of development summarized above

have been described for various species, but it appears that most of these deviations
are misunderstandings caused by lack of detailed observations. One exceptional
type of metamorphosis has, however, been described in detail on the basis of sec-
tions, viz., that of the brackish-water species Victorella muelleri and Bulbella ab-
scondita (Braem, 1951).
The embryos of both species develop in pockets formed by the epithelium of
the vestibule. The rather late embryo of Victorella muelleri (Fig. 71 A) has the usual
apical and pyriform organs, a small adhesive organ and, between the two last-
mentioned organs, a small invagination which may be interpreted as the storno-
daeum. The corona is, however, contracted and the epithelium above the corona
cells forms a thin two-layered membrane below the hyposphere of the larva. A
stage like this has not been described in any other eurystome larva, but Calvet
(1900, pI. 10, fig. 7) has pictured a section of a late embryo of Cryptosula pallasiana
in which a similar infolding of the corona is seen, although the epithelium above
296 CLAUS NIELSEN
the corona does not close below the hyposphere. Another exceptional feature of
the embryo and larva of Victorella is a ring of cilia encircling the stomodaeal
invagination and the adhesive sac, but not the pyriform organ.
At a later embryological stage the epithelial membrane opens and the corona
folds out.
The free-swimming larva resembles the normallecithotrophic eurystome larva
(e. g., Alcyonidium polyoum) except for the "extra" ring of cilia.mentioned above
(Fig.7lB).
After a very short free-swimming phase the larva starts to creep on the sub-
stratum. At the settling the adhesive sac everts and becomes pressed against the
substratum (compare Fig. 71 D). The corona cells become infolded in the usual
way but in this case the infolding proceeds further and after retraction of the ad-
hesive sac the epithelial fold above the corona closes completely, in contact with
the substratum. The newly settled larva (Fig. 71 C) thus fully resembles the em-
bryonic stage described above (Fig. 71 A). Braem (1951) is of the opinion that the
adhesive sac secretes a chitinous substance which glues the larva to the substra-
tum. The apical organ becomes retracted and the polypide formation and the
degeneration of the larval organs do not seem to deviate from those of other
eurystomes described earlier.
The larva of Bulbella abscondita resembles that of Victorella muelleri but has
a very small apical organ, a larger stomodaeal invagination, and lacks the ring of
cilia at the hyposphere. The settling takes place in the very same way as that of
Victorella, described above.
Budding
The formation of the polypide bud in the eurystomes is clearly in need of further
investigation.
All papers from this century agree that the primordium of the bud starts as a
thickening of the one-layered ectoderm (Ladewig, 1900: Bugula; Romer, 1906:
Alcyonidium; Agatz, 1912: Membranipora; Herwig, 1913: Alcyonidium; Soule,
1954: Pherusella, Bowerbankia; Bobin, 1958: Bowerbankia). The internal side of
this thickening becomes covered by a thin layer of cells (mesoderm), but it is not
clear how this layer is form~d. Some authors believe that these cells originate
entirely or in part from the ectoderm (Romer, 1906: Alcyonidium; Herwig, 1913:
Alcyonidium; Soule, 1954: Pherusella, Bowerbankia; Bobin, 1958: Bowerbankiai,
while others believe that they originate from the mesoderm (Ladewig, 1900:
Bugula; Brien & Huysmans, 1938: Bowerbankia; Lutaud, 1961: Membranipora).
A small cavity is formed between the ectoderm cells of the small bud, and a
constriction divides the two-layered sac into a frontal portion which gives rise to
the atrium and the tentacles and a deeper-lying portion which forms the digestive
tract. This constriction is by most of the older authors said to be formed from the
oral end of the polypide bud, leaving a permanent opening between the atrium
and the rectum-intestine-stomach through the anus, while a secondary connection

later on forms between the stomach and the oesophagus which, in turn forms as
a small pouch from the atrium (Haddon, 1883: Carbasea; Barrois, 1886: Schizo-
porella; Davenport, 1891: Paludicella; Calvet, 1900: several species; Agatz, 1912:
Membranipora; Herwig, 1913: Alcyonidium). Soule (1954) states, however, that
in Pherusella and Bowerbankia the oesophagus-stomach-intestine forms as a pro-
trusion from the oral end of the atrium and that the rectum is formed as a separate
invagination from the "upper" part of the atrium.
The ganglion forms as a small invagination of the ectoderm at the limit between
the oesophagus and the anal pair of tentacles (Calvet, 1900).
The septum separating the new zooid from the parental zooid forms simul-
taneously with the polypide bud. A ring-shaped infolding of the ectoderm delimits
the new zooid and secretes the cuticle between its two layers. The fold constricts
and leaves only one or a few small pores in which a plug of specialized cells is
soon formed (Calvet, 1900; Brien & Huysmans, 1938; Silen, 1944c; Bobin, 1962).
Secondary openings in the walls between adjacent zooids develop in several species
(Silen, 1944c).
CYCLOSTOMATA
Embryology
Fertilization has not been observed.
The development from the egg to the ancestrula (Figs 72-73) has been dis-
cussed in an earlier paper (Nielsen, 1970). The single egg cell of a gonozooid di-
vides and forms a rounded mass of cells, the primary embryo, 'which buds off
secondary embryos (tertiary embryos may sometimes be formed). Cell layers
cannot be distinguished in the primary embryos, but in the secondary embryos an
outer and an inner layer of cells soon differentiate. A cavity forms in the inner cell
mass and one side of the embryo invaginates ; this large invagination later on
develops into the adhesive sac of the larva. A wide belt of cilia develops above this
invagination, and the area above this becomes covered by a thin cuticle. The pe-
ripheral part of this cuticle-covered area folds back over the central area, and the
ciliated epithelium thus covers the whole outer surface of the mature larva.
At the metamorphosis the adhesive sac everts in contact with the substratum
and the infolded cuticle-covered epithelium folds out again. The edge of this epi-
thelium unites with the edge of the everted adhesive sac and the cuticle thus covers
the whole upper surface of the metamorphosed larva. The ciliated outer epithelium
of the larva has become enclosed in a ring-shaped cavity.
The inner cell layer below the central part of the cuticle-covered epithelium
increases in thickness, becomes two-layered and folds together as a sac, the poly-
pide bud. At the same time a small invagination develops from the center of the
epithelium with the cuticle forming the primordium of the vestibule. The lower
298 CLAUS NIELSEN
100~
po
FIG. 72. Sections of embryos and settling larvae of Crisia. A, a young primary embryo; B, an ol-
der primary embryo giving off secondary embryos; C, a secondary embryo with two distinct
cell layers; D, an older embryo with developing cilia and cuticle; E, a free-swimming larva; F,
a settling larva; G, a newly settled larva; H, a young primary disc. A, D-H Crisia eburnea, B-C
C. ramosa. A-C redrawn from Harmer (1893) (not exactly to scale), D-H after Nielsen (1970). as,
adhesive sac; cu, cuticle; de, degenerating ciliated cells; po, cells to form the polypide bud; se,
secondary embryo; ve, cells to form the vestibule.
tm
FIG. 73. Polypi de formation in Crisia

eburnea. A, the polypide bud has be-
come two-layered; B, the polypide bud
has become sac-shaped; C, the prin-
cipal parts of the' alimentary canal and
the invagination to form the .ganglion
can be recognized. After Nielsen (1970).
dc, degenerating ciliated cells; ga, in-
vagination to form the ganglion; ip, in-
ner layer of the polypide bud; op, outer
layer of the polypide bud; ph, pharynx;
st, stomach; te, tentacle; tm, terminal
membrane; ve, vestibule.
st ga
part of the polypide bud stretches, bends backwards like a U below the upper part
of the po1ypide bud and differentiates into the pharynx and stomach-intestine-
rectum. The uppermost part of the po1ypide bud everts and forms the thickened
base of the lophophore. The ganglion forms as a small invagination ofthe epithelium
of the anal side of the base of the lophophore. The tentacles develop as protrusions
from the lophophore base. The outer layer of the po1ypide bud differentiates partly
into the "mesodermal" lining of the po1ypide and partly into the so-called mem-
branous sac. The retractor muscles of the po1ypide originate at the wall of the cystid
and insert on a ring-shaped thickening of the basal membrane of the lophophore.
Budding
The budding of the cyclostomes has only been rather poorly described. Harmer
(1898) and Robertson (1903) made some few observations, and Borg (1923, 1926)
gave a more detailed but poorly illustrated description based on studies of several
species. He observed the primordia of the polypide buds in the shape of small
rounded thickenings in the epithelium of the growing edge of the colonies. The
300 CLAUS NIELSEN
thickening consists of some cells which are in contact with the terminal membrane
and some cells lying below these; one of the inner cells has a very large nucleus
and the following development shows that it is the germinal cell. This thickening
sinks down below the terminal membrane and soon folds together as a small
narrow sac surrounded by a well-defined layer of cells; the germinal cells can still
be distinguished at the lower side of the bud. The outer cell layer differentiates
into two cell layers, one which lies in contact with the sac, and another which
forms the "membranous sac". The epithelium with its cuticle above the bud sinks
down and forms the vestibule. At this stage starts the formation of the cystid wall
separating the new polypide from the common lumen of the growing zone of the
colony; it develops as an infolding of the epithelium which secretes the calcareous
body wall.
Borg (1926, p. 230) states that the polypide bud constricts at the "equator",
leaving only a small opening between a proximal and a distal cavity; this opening
is said to represent the anus of the adult polypide. The proximal part should dif-
ferentiate into stomach, intestine and rectum, while the distal part should give
rise to tentacles and pharynx. The communication between the pharynx and the
stomach should thus be formed at a later stage. This description is in contrast to
my own description of the formation of the polypide in the ancestrula (Nielsen,
1970, see above).
The further development (Borg, 1926) closely follows the development of the
ancestrula described above.
PHYLACTOLAEMATA
Embryology
Fertilization has not been observed in any of the phylactolaemates but I find it
probable that cross-fertilization occurs here as it does in the eurystomes. The egg
becomes fertilized already in the ovary in Lophopus (Marcus, 1934). The early
embryology has only been studied by few authors; Plumatella has been studied by
Davenport (1891), Kraepelin (1892), Braem (1897), and Brien (1953); Cristatella
by Davenport (1891); Fredericella by Braem (1908), and Lophopus by Marcus
(1934). These studies show a high degree of similarity between the species, but sev-
eral important questions have remained unanswered.
The fertilized egg enters the embryo sac (Hyman, 1959), an invagination of
both layers of the body wall, and comes to lie totally surrounded by ectodermal
cells. Polar bodies have not been observed, and Marcus (1934) observed that the
spindles of the meiotic divisions may have various orientations.
The cleavage results in an irregular mass of cells (Fig. 74A) which is almost
compact until a stage of about 30 cells. A sort of gastrulation from the side facing
the exterior (the distal end) has been described in Cristatella and Plumatella by
Davenport (1891) and in Plumatella by Braem (1897), but has not been observed
kz
em
em
pi
FIG. 74. Development of Plumatella fungosa. A, a section of an embryo consisting of a few cells,
enclosed in the embryo sac; B, a section of an early two-layered embryo with some "Kopfzellen";
C, a section of a two-layered embryo; D-F, sections of embryos with placenta and developing
buds; G, a large embryo inside the maternal zooid; H, a free-swimming "larva", the arrow in-
dicates the swimming direction; I, a settling specimen; K, a young colony still showing the in-
vaginated ciliated epithelium of the larva. A-C, G-K after Brien (1953), D-F redrawn from Braem
(1897). Not to scale. dc, degenerating ciliated epithelium; em, embryo; ga, ganglion; kz, "Kopf-
zellen"; pb, polypide bud; pl, placenta.
302 CLAUS NIELSEN
by the later authors. The invaginated cells should then degenerate (Braem, op. cit.),
and all authors except Davenport (1891) have observed a stage resembling an
elongated one-layered sac. In Fredericella, Braem (1908) observed some large cells
("Kopfzellen") at the distal end of the embryo; their number was not constant;
now and then they were totally absent, and they disintegrated after some time.
Braem (op. cit.) interpreted them as the entoderm cells and the whole embryo as
an exogastrula. Brien (1953) observed a similar stage in Plumatella (Fig. 74B),
but denied that the large distal cells should be regarded as entoderm cells. The
embryo then becomes two-layered (Fig. 74C). In Plumatella, Braem (1897) ob-
served that the cells of the distal part of the embryo were large and gave off cells
forming the inner layer. These cells first formed a closed vesicle in the distal end,
but this vesicle soon enlarged so that the whole embryo became two-layered. In
Fredericella, however, the proximal cells are the largest and the inner layer origi-
nates from this region as a compact mass which soon becomes hollow and spreads
to the distal end (Braem, 1908). Marcus (1934) was unable to find any "Kopfzel-
len" in Lophopus, but observed some loose cells around the two-layered embryo;
he believed that these cells represented the primary entoderm.
An area of the embryo comes into intimate contact with the embryo sac and
a sort of placenta develops. This placenta forms a ring above the middle of the
embryo in Plumatella (Kraepelin, 1892; Braem, 1897) (Fig. 74D-F), but occupies
the distal tip of the embryo in Fredericella (Braem, 1908).
The embryo now starts budding (Fig. 74E-G); a number of buds develop at the
distal part of the embryo in the same way as the buds of the adult colonies (de-
scribed below).
The number of buds varies among the species; Fredericella develops only one
bud (Braem, 1908; Brien, 1953), whereas between one and 25 buds have been
recorded for members of other genera (see Rogick, 1939).
A ring-shaped fold (the mantle) develops below the budding zone (and below
the ring placenta in Plumatella); it extends over the budding zone (and the pla-
centa) (Fig. 74G) and finally covers the whole distal part of the embryo, only
leaving a small opening at the top. The external side of the embryo develops a fine
ciliary cover and the larva is now ready for liberation. Marcus (1926b) observed
0
that the larva rotates 180 and becomes liberated with the "proximal" end first.
The larva (Fig. 74H) swims for a period of a few minutes to about one day;
in rotates through the water with the pole opposite the polypides in front (Braem,
1897). Marcus (1926b) described a net of epithelial sense cells with a concentra-
tion of cells at the anterior pole (in the swimming direction).
At the settling the larva attaches with the pole opposite the polypides and
retroflexes the mantle fold against the substratum (Braem, 1890). The whole cili-
ated epithelium finally becomes enclosed in an invagination at the base of the
young colony, which is attached to the substratum with the epithelium of the upper
part of the inner side of the mantle fold. Brien (1953) gives a similar description,
the only difference being that the newly settled larva adheres to the substratum
by its side (Fig. 74I-K). The young colony may now protrude the lophophores,
and this is sometimes seen already in the free-swimming stage (see Brien, 1960,
fig. 1003).
Budding
In the Phylactolaemata three types of buds are formed: a) buds formed from the
two-layered embryo still contained in the embryo sac; b) buds formed from the
adult colonies; c) buds formed by the germination of the statoblasts. The three
types of buds are, however, formed in the same way, as seen from the descriptions
FIG. 75. Budding of the phylactolaemates, A-B, formation of the two-layered, sac-shaped bud
through invagination from the cystid wall in Plumatella fungosa; C-E, formation of the funiculus
and the duplicate bud in Plumatella [ungosa; F-G, the formation of the alimentary canal in Cri-
statella mucedo, slightly modified to clarify Davenport's interpretation; H-I, the formation of the
alimentary canal in Pectinatella gelatinosa. A-E after Brien (1953), F-G redrawn from Davenport
(1890), H-I redrawn from Oka (1891). Not to scale. db, duplicate bud; fu, funiculus; 10, lopho-
phore; ph, pharynx; re, rectum; st, stomach.
304 CLAUS NIELSEN
in the literature (C = Cristatella; F = Fredericella; Pe = Pectinatella; PI = Plu-

matella): Nitsche (1875: C,PI: a); Davenport (1890: C: b; 1891: C,PI: a); Braem
(1890: C, PI: b, c; 1897: PI: a; 1908: F: a; 1913: C, Pe: c); Kraepelin (1892: C,
PI: a, b); Herwig (1913: PI: b); Brien (1936: F, PI: b; 1953: C, F, PI: b). Only the
account given by Oka (1891 : Pe: b, c) shows an important divergence (see below).
The bud originates as a two-layered invagination from the body wall (Fig.
75A-B). The bottom of the invagination grows and a string of cells separates
from its "mesodermal" layer, forming the funiculus (Fig. 75C). A few cells from
the ectoderm at the attachment of the funiculus enter this, and later on these cells
form the epithelial cover secreting the wall of the statoblasts. The polypide bud
gives off the so-called duplicate bud, and its lower part elongates parallel to the
cystid wall (Fig. 75D-E). The portion of this elongation closest to the funiculus
forms the region of the mouth while an expansion from the opposite region forms
a diverticulum representing the rectum-stomach (Fig. 75 F-G). This means that
the anus is a permanent opening while a secondary opening at a later stage forms
between the diverticulum and the mouth region, possibly at the limit between the
oesophagus and the cardia. Oka (1891) states, however, that the diverticulum
forms from the mouth region and that the anus forms secondarily (Fig. 75 H-I).
None.of the recent papers give information on this point, which seems in need of
new investigations. The tentacles develop from a transverse thickening of the
epithelium which grows out to form the lophophore. The ganglion develops as a
small diverticulum from the epithelium of the posterior part of the mouth region.
The incomplete partitions between the zooids are simple infoldings of the
body wall protruding into the common body cavity of the colony.
DISCUSSION
The three groups of the Ectoprocta show considerable variation in their develop-
ment. The Eurystomata comprises both types with small eggs and planktotrophic
larvae and types with large eggs and larvae lacking a gut. The embryology shows,
however, that these differences are merely variations over a common theme, and
several intermediate types are also found. The most specialized larvae (see dis-
cussion p. 310), as for example those of Bugula, have a ring of very high prototroch
cells covering almost their whole surface (see Calvet, 1900). The apical organs and
the pyriform organs are clearly homologous in all the different types. The adhesive
sac is likewise present in all types; it evaginates and furnishes the secretion which
glues the larva to the substratum. Upon settling the prototroch becomes enclosed
in a cavity, and all larval organs degenerate.
The Cyclostomata are unique among the ectoprocts in having polyembryony.
These larvae lack any trace of a gut and appear highly specialized. They can be
regarded as a Bugula-like type in which both the apical organ and the pyriform
organ have disappeared. This comparison is strongly supported by the metamor-
phosis, which is almost identical with that of eurystomes such as Electra and
M embranipora.
The embryology of the Phylactolaemata is likewise highly modified. The
development takes place in an embryo sac which is very similar to the embryo sac
found in the eurystomes Labiostomella and Sundanella (Silen, 1944a). The present
knowledge does not give any direct information on the orientation of the embryos
and larvae, and it is unclear how the inner cell layer is being formed. The develop-
ing buds indicate, however, that the larvae must be considered as cystids and the
two cell layers may, therefore, be called ectoderm and mesoderm. The settling of
the larvae seems to support this interpretation; the whole ciliated epithelium
becomes enclosed in a cavity inside the young colony. The young colony is not
attached to the subtratum with an evaginated adhesive sac but with the region
"above" the prototroch. This is different from the typical pattern in most of the
eurystomes and in the cyclostomes, but the same region of attachment is found in
Victorella and Bulbella (see Fig. 71). It thus appears that Lemche's (1963) theory of
deriving the phylactolaemates from the rhizostomatous medusae cannot be main-
tained. It is mainly based on the assumption that the young colony settles with the
apical pole and this is in no way proved. The close similarities in the settling (and
the budding, see below) of the phylactolaemates and the other ectoprocts strongly
support the concept of a common ancestry.
The above descriptions of the development of the various types have shown
that the germ layers are very difficult to follow, and I have deliberately tried to
avoid the use of the word mesoderm.
The budding of the three ectoproct groups shows distinct similarities. The
whole epithelium of the alimentary canal clearly originates directly from the ecto-
derm of the budding zone (except in the cyclostomes where the origin of the cells
forming the polypide in the ancestrula is uncertain).
The ganglion is in all cases formed as a small invagination from the ectoderm of
the posterior side of the mouth region. The partitions between the zooids form
as flat invaginations from the body wall. Some of the differences which can be
found by comparing the summaries above may even be illusive and due to lack of
detailed investigations. This is probably the case with the differences between the
formation of the different parts of the digestive tract. It does not seem probable
that the anus should be the permanent opening between the atrium and the gut
and the mouth a secondary opening in some eurystomes while the opposite has
been described in other species. It also seems quite improbable that the same dif-
ference should exist between colonies of Pectinatella from Japan and Germany.
Also the origin of the layer of cells covering the exterior of the gut differs ac-
cording to the various authors. It is clear that it originates directly from the inner
layer of the cystid in the phylactolaemates but it is quite unclear how it originates
in the eurystomes. If my interpretation of the membranous sac of the cyclostomes
as the "mesoderm" of the cystid is correct (Nielsen, 1970), it implies that the
20
306 CLAUS NIELSEN
"mesoderm" of the buds must be formed from the ectoderm, because the mem-
branous sac is not in contact with the budding zone. It is from the above state-
ments quite clear that the budding of the ectoprocts is badly in need of further
investigation.
PHYLOGENETIC CONSIDERATIONS
THE ORIGIN OF THE ENTOPROCTA
The entoprocts have knocked about a good deal in the zoological system. It
appears, however, that many of the various positions have been based on nega-
tive evidence, namely that the entoprocts do not fit into the more well-defined
groups. Several positions are not the results of phylogenetic considerations. Some
authors have regarded the entoprocts as neotenous ectoprocts (e. g., Lameere,
1931; Marcus, 1958), but there seems to be no direct evidence for this theory. The
opposite theory, namely that the ectoprocts have evolved from an entoproct-like
ancestor, has been proposed by several authors and will be discussed in the next
chapter.
The entoproct larva is a typical trochophore, and in the larvae lacking a foot
(e. g., Loxosomella elegans and Loxosoma pectinaricolay the whole ciliary system
is very similar to that of a polychaete larva (see Fig. 76). The spiral cleavage and
the whole organogenesis of the larva closely resemble those of polychaetes, mol-
apical organ
prototroch prototroch
anus
FIG. 76. A, lateral view of a six days old trochophore larva of Pomatoceros triqueter; after Segrove
(1941); B, lateral view of a newly released larva of Loxosomella elegans.
luscs, sipunculids, and echiuroids. The frontal organ seems to be a structure char-
acteristic of the entoproct larva, but it perhaps corresponds to the cerebral ganglion
of the polychaetes, which in some types is formed from a pair of invaginations
above the prototroch (Akesson, 1962; Anderson, 1966), and the cerebral ganglion
of the molluscs, which, for example, in Haliotis is formed in the same general
region (Crofts, 1937). Eyes resembling those of the loxosomatid larvae are found
in many of the trochophore larvae of the just-mentioned groups. The common
ancestry of these groups has been more or less accepted by several authors (e. g.,
Hatschek, 1891; Bek1emischew, 1958) and will not be discussed further here.
Balfour (1880, p. 255) was apparently-the first to propose that the entoprocts
had evolved from a trochophore-like ancestor "which became fixed in the adult
by the extremity of their pre-oral lobe". The same opinion was held by Ehlers
(1890, p. 163), MacBride (1914, p. 405) and Brien & Papyn (1954). All these authors
mention the analogous settling of the cirriped larva. Jagersten (1968) elaborated
the theory and gave very instructive drawings showing the similarity between the
ciliation of a trochophore and a primitive Ioxosomatid, All these authors had
based their opinion of the settling of the ancestor on theoretical considerations,
but it has now been shown (see p. 272) that several species of Loxosomella actually
settle by means of the contracted frontal organ. Therefore, it now seems justified
to construct a more detailed theory for the evolution of the Entoprocta (Fig. 77):
The ancestor of the Entoprocta was an organism with a pe1ago-benthic life-
cycle. The larva was a typical trochophore with an apical organ, the usual ciliary
bands and a pair of protonephridia as shown in Fig. 77At. The adult crept on a
foot-like enlargement of the neurotroch and had developed a paired sense organ
(the frontal organ) above the anterior part of the prototroch (Fig. 77A.).
The creeping ancestor developed glandular cells around the frontal organ and
became able to attach temporarily to the substratum with this organ. This attach-
ment became permanent and the foot degenerated in the adult; a new ganglion
developed at the ventral side and the apical organ, which is of special importance
in the planktonic phase, degenerated. The resulting organism (Fig. 77 B3 ) has
most of the fundamental features of an entoproct.
Protrusions formed on the girdle of prototroch cells and developed into the
tentacles, each with a branch of the adoral ciliation on their "frontal" side. In the
extant entoprocts the row of lateral cilia of the tentacles ("prototroch") is contin-
uous with the row of cilia at the edge of the atrial groove ("metatroch") at the
anal side, where new tentacles may develop, each bearing an extension of the pro-
totroch (Fig. 77 Co). This means that the tentacles of the entoprocts do not form
a circle but a horseshoe, and further that these organisms are no more "entoproct-
ous" than the phylacto1aemates (see also Fig. 80). The budding probably developed
soon after the sessile stage had been reached.
The metamorphosis of the extant Loxosomatidae involves a temporary clos-
ing of the atrium and a reorganization of the ciliary apparatus and the organs of
20·
308 CLAUS NIELSEN
anus
prctotroch
adoral cilia
metatroch
gastratroch
mouth
A,
==:> phylogeny
..... ontogeny
'""""'"~III1'" caenogenesis
t C4
~11I11I11l111111111I11'
e
[f) 11111111111111111111 1•
~
t C
3
.~"'''';IIII''
t t t C
2
t
(~) C~J
FIG. 77. A hologenetic schema of the evolution of the Entoprocta from a creeping, trochophore-
like ancestor. The most important steps in the evolution have been numbered according to their
appearance (white numbers on black circles): I, the creeping "trochozoon" develops glands around
the frontal organ, enabling it to attach to the substratum and lift the prototroch; 2, the ciliated
foot degenerates in the adult; 3, protrusions develop from the prototroch and form the tentacles;
4, the atrium closes for a short period just after the settling and the ciliated epithelia become
reorganized; 5, glands, probably originally connected with the creeping, become specialized so
that they may glue the metamorphosing larva to the substratum, and the larva now settles with
the region above the retracted prototroch. The development of the larvae of Loxosomella and
Pedicellina takes place inside the egg membrane, and the stages corresponding to A 1 and B1 are
modified; I have therefore pictured swimming, fully grown larvae instead.
the lower side of the larva (Fig. 77C g ) . This must be regarded a caenogenetic
specialization (a specialization of a juvenile stage) because a primary closing of the
atrium in the adult must evidently be of negative selective value; it would not
only prevent the adult from taking up food but also from reproducing. The de-
generation of the ciliary apparatus and the formation of a new one of similar
structure from a neighbouring epithelium appear to be analogous to the formation
of the new tentacles at the metamorphosis of the actinotrocha larva. Although the
ciliary bands of the larva are not directly taken over by the adult, their detailed
similarity seems to make it permissible to use the ciliation of the adults in com-
parisons with the trochophore. The budding and other specializations of the
larvae of severalloxosomatid species have been discussed earlier (see pp 272-275).
In the Pedicellinidae the metamorphosis has become further specialized; the

larva has developed three pairs of glands from the epithelium of the foot and at
the settling it uses the secretion from these glands to glue the row of cells above
the contracted prototroch to the substratum. The slight rotation of the digestive
tract in the metamorphosing Loxosomella has in the Pedicellinidae become al-
most 180 0 (Fig. 77 Dg-D.). Here again it can be taken for granted that the meta-
morphosis is the result of a caenogenetic specialization since it seems most un-
likely that selection should favour a direct evolution which renders both gut and
generative organs of the adult non-functional.
THE ORIGIN OF THE ECTOPROCTA
Before discussing the ancestry of the Ectoprocta it seems appropriate to point out
that the polypide in all extant ectoprocts is formed through a budding process
from an area which probably in all cases corresponds to the episphere of the cy-
phonautes larva. Thus, the gut of the polypide has nothing to do with the gut of
the planktotrophic larva. The orientation of the polypide can therefore not be
based on embryological evidence, but must be based on comparisons with other
animal types. In discussions of relationships between ectoprocts and other groups
it is, therefore, clear that to state, for example, that "the ganglion of the ectoprocts
is dorsal" (Cori, 1936) is merely arguing in a circle. The commonly accepted orien-
tation of the ectoprocts, viz., with the dorsal side up, is based on comparisons with
the phoronids.
It seems natural to believe that the ancestor of the ectoprocts was a solitary
animal in which the alimentary canal of the larva was retained in the adult. It
seems furthermore unquestionable that the colony formation developed after the
ancestor had become sessile or at least semisessile. The gut of the cyphonautes
larva is by most authors (Cori, 1941; Marcus, 1958; Hyman, 1959; Brien, 1960;
Jagersten, 1968) believed to be homologous with the gut of the trochophore larva.
Silen (1944 a, pp 87-89) admits that a larval gut has been present in the larva of the
early ancestor, but believes that the ectoprocts at an early stage became brood-
310 CLAUS NIELSEN
protecting and that the larvae lost the gut. The gut of the cyphonautes larva
should, therefore, represent a caenogenetic specialization in types which had sec-
ondarily lost the habit of brooding the embryos. This is based on the conception
that Membranipora and Electra, which have the typical cyphonautes larva, are
not primitive but secondarily simplified types. The lecithotrophic larval forms with
traces of a gut (e. g., Flustrellidra) are considered "without importance for the
present discussion" (op. cit., pp 89-90). There is, however, no reason to believe
that a specialization of the adult animal necessarily is connected with a special-
ization of the larva. To me it seems clear that the lecithotrophic larva with a more
or less developed alimentary canal (see pp 289, 292) indicates that the ancestral
type had a functional gut, and that the cyphonautes larva directly represents this
ancestral type of larva.

Several authors have compared the ectoprocts, especially the phylactolaemates,
with the phoronids, and found so many similarities between the two groups that
they have united them (together with the brachiopods) into the group Tentaculata
or Lophophorata (e.g., Cori, 1941; Marcus, 1958; Hyman, 1959; Dawydoff &
Grasse, 1959; Brien, 1960; Siewing, 1967; Jagersten, 1968). Some authors (Cori,
op. cit.; Silen, 1944a; Beklemischew, 1958) derive the ancestral solitary ectoproct
from a Phoronis-like type which is able to retract the lophophore, a theory sup-
ported by the fact that Phoronis ovalis apparently is able to retract its anterior end
(Harmer, 1917). These authors ascribed the development of the colony formation
to the power of regeneration of the anterior part of the body, which is easily dam-
aged and which in the ectoprocts often degenerates (to form a brown body) while
a new polypide soon develops. The life-cycles of the two types were not compared,
and serious difficulties appear when one tries to derive the ectoproct type of life-
cycle from the phoronid type, which seems primitive. The tentacles of the adult
phoronids develop from or in direct contact with what must be considered the
metatroch of the actinotrocha larva (Dawydoff & Grasse, 1959). By the meta-
morphosis of the ectoproct larva (seen clearly in the eurystome larvae) the pro-
totroch and the whole hyposphere become enclosed under the episphere, which
comes into contact with the substratum (or the evaginated adhesive sac); the
episphere then gives rise to the buds. It is, therefore, very difficult to imagine how
selection should favour the evolution of a phoronid-like, solitary "probryozoan"
with a metamorphosis similar to that of the extant ectoprocts; this would involve
the enclosure of the tentacles below a fold of the episphere, rendering the animal
incapable of taking up food and of reproducing. The only possibility of "saving"
this theory would be to propose that budding had developed already in the pho-
ronid-like ancestor. However, the buds of the extant ectoprocts form from the
episphere of the larva, which corresponds to the narrow area inside the ring of
tentacles of the phoronids, and budding from this area seems incompatible with
the general phoronid organization. If the buds had been formed from the sides of
the body as in Phoronis ovalis (Harmer, 1917), they, too, would become enclosed
creeping organ A
postoral cilia
c
attachment glands
FIG. 78. Schemata of hypothetic adult ancestral types of the tentaculates. A, a vagile ancestor
sliding along the substratum by means of a preoral, ciliated creeping organ; B-C, alternative
schemata of the sessile protentaculate. After Jagersten (1969).
by the metamorphosis. It can also be mentioned that the young buds of Phoronis
ovalis contain a side branch from the descending branch of the digestive tube of
the mother animal and that this branch gives rise to the independent gut of the
fully developed bud. This is in contrast to the budding in the ectoprocts in which
the whole alimentary canal is formed from the ectoderm, a type of budding which
is elsewhere only described from entoprocts (see pp 276-277) and Cephalodiscus
(Masterman, 1898).
Thus, it seems impossible to derive the ectoprocts from a phoronid-like ancestor.
In a very thought-provoking book Jagersten (1968) points out that the whole
life-cycles of the animals must be considered in phylogenetic discussions. In theories
involving a derivation of one type from another it is a prerequisite that all inter-
mediate stages have been viable. This principle has been used above to reject the
theories of a derivation of the ectoprocts from a phoronid-like ancestor. Jager-
sten (op. cit.) constructs a perfectly viable "protentaculate" with a cyphonautes-
like larval stage (see Fig. 78), and it seems quite easy to derive a solitary "pro-
bryozoan" from the organism in Fig. 78 C. The very same arguments given above
against the Phoronis-theory apply when the extant colony-forming ectoprocts are
to be derived from this organism. It seems easier to derive an ectoproct-like type
from the animal pictured in Fig. 78 B if this organism lost at least part of the shell
and started budding from the episphere. Jagersten hardly discussed the origin of
the budding, but only states that this budding is analogous to the budding of the
Entoprocta (op.cit., pp 46-47). It can, however, be argued that the organisms pic-
tured in Fig. 78A-B are so little differentiated that they may also serve as ancestors
to many other types, for example the Mollusca. Jagersten (op, cit., p. 65) explains
312 CLAUS NIELSEN
the similarities with the molluscs as a convergence and bases his rejection of the
apparent relationship on the assumption that the locomotory organ of the vagile
ancestor was the preoral organ and not a ventral "foot". He does, however, picture
the ancestor with a ventral ciliation (see Fig. 78A) and I see no reason why this
organ should not be locomotory as it is in a number of other larval types (larvae of
entoprocts, polychaetes, molluscs and pogonophorans). In my opinion, Jagersten's
ideas cannot be cited in support of the theory of a close relationship between ecto-
procts and phoronids.
A "probryozoan" resembling that in Fig. 87A was already figured by Ostrou-
moff(1885b), but his hypothetical form had a small ciliary plume above the mouth
instead of a large locomotory organ. It was believed to metamorphose as the ex-
tant ectoprocts and to bud from the episphere.

The other commonly discussed theory for the derivation of the ectoprocts
regards an entoproct-like form as the ancestor. This theory was proposed by Bal-
four (1880) and furthered by Harmer (1885, 1886, 1887), based on his investi-
gations on the larvae of Loxosomella and Pedicellina; it was also discussed by
Ehlers (1890). It stresses the similarity between the larvae of the Entoprocta and
the Ectoprocta (as did Seeliger, 1906; Czwiklitzer, 1908; and most of the later
authors) and interprets the ectoproct colony as a sort of entoproct larva which
through the metamorphosis had lost the gut and which had already started the
budding (Harmer, 1886, p. 260). This theory comes close to that of Ostroumoff
(1885b), although this author did not compare his hypothetical form with an en-
toproct larva. Also Buddenbrock (1933) suggested a relationship of this type.
The recent observations on budding in entoproct larvae (see pp 272-273)
make it worth while to elaborate the just-mentioned theory and to reconsider the
criteria used by several authors to separate the Entoprocta from the Ectoprocta.
In the preceding section I have tried to show how the type of metamorphosis
of the Pedicellinidae has evolved from the type shown by, for example, Loxosomella
harmeri. If we now compare the settling of Pedicellina with that of Electra (Fig.
79) it will easily be seen that the first stages of this process are very similar in the
two types: The edge of the episphere just above the prototroch comes into con-
tact with the substratum and the whole digestive tract becomes enclosed; the pro-
totroch and the larval sense organs (apical organ, frontal organ, pyriform organ)
degenerate in both types. The most important difference seems to be the mode
of attachment: In Pedicellina it appears that the three pairs of glands associated
with the foot release the secretion which glues the constricted area above the pro-
totroch to the substratum; in Electra the basal wall of the ancestrula is formed by
the eversion of the glandular adhesive sac whose edge comes into contact with the
cells above the infolded prototroch. There is, however, a type of eurystome, here
represented by Victorella (see also p. 295), in which the adhesive sac becomes re-
tracted after having released its secretion, as in Pedicellina, and where the general
morphology of the newly settled individual thus is almost identical with that of a
co
FIG. 79. Schemata of the larvae and the settling of Pedicellina, Victorella and Electra. an, anus;
ao, apical organ; as, adhesive sac; co, corona; fg, foot gland; mo, mouth; po, pyriform organ;
pr, prototroch; st, stomach.
314 CLAUS NIELSEN
newly settled Pedicellina (Fig. 79). It is in this connection without importance that
the larva of Victorella lacks the gut because similar lecithotrophic larvae without
a digestive tract are found among the entoprocts (e. g., Loxosomella viviparay,
0
The digestive tract of the Pedicellina larva rotates 180 and becomes the gut
of the first adult individual in a colony. In the ectoproct larvae which have a di-
gestive tract this degenerates completely and a new one forms through the budding
(a pair of buds is formed simultaneously in Membranipora). The gap between
these two types is bridged by some of the Loxosomatidae. In Loxosomella leptoclini
a pair of buds sprouts from the episphere of the larva; these buds are released from
the larva, which during the growth of the buds is loosely attached to the substratum
while its internal organs slowly degenerate. In other Ioxosomatid larvae such as
those of Loxosomella vivipara and Loxosoma jaegersteni the buds are formed in
invaginations from the epithelium and lie fully formed inside the larva, like the
polypides inside the larvae of the phylactolaemates.
The budding process is very similar in the Ectoprocta and the Entoprocta
(see below). All the individuals in the colonies are connected with each other, and
the cuticular walls between the individuals are only incomplete partitions of the
common tissue.
These considerations leave one with the impression that the ancestor of the
Ectoprocta was an organism with a life-cycle very similar to that of Pedicellina.
In a colonial organism of this type it is not imperative that the larval gut retains its
function, and the gut may, therefore, degenerate after the metamorphosis of the
larva (analogous to the degeneration in the larva of Loxosomella leptoclini). The
budding may become internal (as in Loxosomella vivipara and Loxosoma jaeger-
steni) and an organism with these characteristics only needs few modifications to
.resemble-a typical ectoproct. These important modifications needed for transform-
ing a Pedicellina-like ancestor into a primitive ectoproct have been realized in-
dependently in various members of the Loxosomatidae, and there seems to be no
difficulties in combining these modifications and realizing them in an organism
resembling the Pedicellinidae.
It is not possible to state the succession of the various steps involved in the evo-
lution of the pro-ectoproct from the entoproct-like ancestor and I have, therefore,
refrained from making a graphic representation of this process.
When the pro-ectoproct stage has been reached it is possible for the larva and
the adult to become modified in different directions. A specialization of the larval
organs is not necessarily combined with an alteration of the morphology of the
adult polypide, and the polypide may become specialized without this influencing
the organization of the larva.
The development and adult anatomy of the ento- and ectoprocts will be dis-
cussed in the following in the light of the above hypothesis, with special attention
being given to the detailed argumentations of Cori (1936) and Marcus (1939) on
the same subject.
Embryology
The embryology of the Ectoprocta shows great variation (discussed earlier), but
for a comparison with the Entoprocta it appears sufficient to concentrate on the
types found within the Eurystomata.
In the Entoprocta some species have spiral cleavage, but this characteristic
pattern is lost in embryos of Loxosomella vivipara beyond the eight-cell stage. In the
Eurystomata cleavage is' of the radial type. This seems to be an important differ-
ence between the two groups, but the cleavage of Loxosomella vivipara shows that
the cleavage type may become modified. Intermediate types between the spiral
and the radial pattern are not known within these groups, but it is known that the
cleavage type may vary within well-defined systematic groups. This is, for example,
the case for the Phoronida, where Rattenbury (1954) found clear indications of a
spiral pattern in the cleavage of Phoronopsis viridis, whereas cleavage is radial in
other species investigated (Hyman, 1959).
In both groups the gastrulation takes place through invagination in the types
having "planktotrcphic larvae, but considerable variation exists in types having
lecithotrophic larvae. The larvae of both groups soon develop a ring of large
prototroch cells and an apical organ. The origin and differentiation of the meso-
dermal organs have not been studied in detail and it seems premature to make any
compansons.
Larvae
The similarities between the larvae of the two groups have been pointed out by
several authors (see above).
The modifications needed to transform a Pedicellina larva into an ectoproct
larva are few. The frontal organ of the Pedicellina larva must disappear, but this
organ has already lost its importance as an adhesive organ in the larvae of Loxo-
somella vivipara, L. leptoclini and Loxosoma jaegersteni, and it appears to have lost
its function as a sensory organ in the larvae of Loxosomella elegans and Loxosoma
pectinaricola, which only have a small frontal ganglion and no protrusible ciliated
sacs (at least in the newly released larvae). The paired nerves from the apical organ
to the pyriform organ in the cyphonautes larva probably correspond to the nerves
from the apical organ via the frontal organ to the prototroch in the larva of Loxo-
soma pectinaricola, and the pyriform organ may be interpreted as the specialized
anterior region of the prototroch. The frontal organ is formed from the episphere,
and therefore I don't think it is possible to homologize the frontal organ with the
pyriform organ as proposed by Seeliger (1906). The foot of the Pedicellina-use
larva must degenerate, leaving only an invagination with the large glands secre-
ting the substance attaching the metamophosed larva to the substratum (the ad-
hesive sac). (The foot of the Pedicellina larva is embryologically formed as an in-
vagination from the epithelium between the stomodaeum and the proctodaeum.)
316 CLAUS NIELSEN
The larvae of the Cyclostomata and Phylactolaemata represent specializations

of the general type exemplified by Electra (see pp 304-305).
Settling and metamorphosis

The entoproct larva which is ready to settle creeps on the substratum and tests it
with the protruded frontal organ. When a suitable spot has been selected the
hyposphere retracts completely and the ring of cells above the prototroch con-
stricts below it (Fig. 79 A). The larvae attach to the substratum by means of
secretions from various glands. In species of Loxosomella this secretion is apparent-
ly provided by a ring of cells around the frontal organ and these larvae attach
with the frontal region. Tn the Pedicellinidae the secretion comes from the three
pairs of foot glands and these larvae adhere to the substratum with the region just
above the retracted prototroch.
The eurystome larva likewise creeps on the substratum before the settling, test-
ing it with the protracted pyriform organ. In types such as Electra, Membranipora
and Flustrellidra the settling larva everts the adhesive sac in contact with the sub-
stratum and retracts the prototroch so that the cells above it come into contact
with the edge of the adhesive sac (Fig. 79 C). In Victorella and Bulbella the adhesive
sac retracts again after having given off its secretion and the cells above the pro-
totroch constrict completely and form the region of attachment (Fig. 79 B), just
as in the pedicellinids. In Bugula and Scrupocellaria, and perhaps in many other
types, the edge of the everted adhesive sac rises along the periphery of the settling
larva and finally constricts completely above it (see Fig. 73).
In the phylactolaemates the whole ciliated epithelium of the settling larva (the
enlarged prototroch) retroflexes and becomes enclosed by the constriction of the
ring of cells originally situated above the ciliated area (Fig. 74); this is quite similar
to the metamorphosis of the pedicellinid larva.
All the entoprocts and ectoprocts pass through a stage in which the prototroch
has become retracted and completely enclosed in a cavity. The prototroch disin-
tegrates and the characteristic single cells, each with a tuft of cilia enclosed in a
vacuole can be found in the body cavity of the metamorphosing animals (not
observed in the phylactolaemates).
The larval gut persists in the adults of most species of the Entoprocta whereas
it degenerates completely after the settling of the cyphonautes larva. The polypide
of the ancestrula of the eurystomes is thus comparable to the first bud developing
on the metamorphosed individual in the entoprocts (see the section on budding).
These detailed similarities in the settling and certain parts of the metamor-
phosis of the Entoprocta and Ectoprocta must be of high phylogenetic significance.
Cuticle
The body wall of the Entoprocta consists of a one-layered epithelium which is
covered by a cuticle except at the frontal side of the tentacles and the atrium. This
cuticle is thickened at the stolons of the pedicellinids and is especially thick at the
elastic joints of the stalk of Barentsia. The biochemistry of the cuticle is almost
unknown, but Hyman (1966) states that chitin is not present.
The cystid of the Ectoprocta is uncalcified in the Ctenostomata and Phylacto-
laemata and calcified in the Cheilostomata and Cyclostomata. The cuticle consists
mainly of protein, but also contains a stereoisomer of true chitin (Ryland, 1970).
The chemical composition of the cystid has been studied by Schopf & Manheim
(1967), Banta (1968) and Bobin & Prenant (1968), but the sparse knowledge of the
composition of the entoproct cuticle makes comparisons premature.
Body cavity
The presence of a "coelom" in the ectoprocts and its absence in the entoprocts
seems to be a highly significant difference, and it has been the most important
reason for separating the two groups entirely.
There is nothing to indicate that the larvae of the ento- and ectoprocts at any
time have had a "coelom".
The adult entoprocts are definitely without a coelom, but a "haemolymph" is
present between the mesoderm cells. A special system of "star" cells at the base
of the calyx has been observed to create circulation of this fluid in Pedicellina,
Barentsia and Urnatella (Emschermann, 1969), and a similar group of cells in
Myosoma is pictured by Franzen (1970b). The loxosomatids lack these specialized
cells.
The body cavity of the adult ectoprocts is not a typical coelom. The mesoderm
layer is incomplete, for example, in the regions of growth (see, e. g., Brien & Huys-
mans, 1938), and some authors, e. g., Clark (1921), even place the group within
the Acoelomata. The formation of the body cavity after the metamorphosis of the
larva is very peculiar: The enclosed epithelium of the corona (prototroch) and the
whole alimentary canal (in the cyphonautes larva) degenerate and leave a cavity
which seems to be lined by only one layer of cells except in the area of the future
polypi de bud. The origin of the mesoderm layer is obscure. This resembles some
of the processes in the metamorphosis of Loxosomella harmeri, Pedicellina cernua
and Barentsia gracilis B. In these forms the cells of the prototroch likewise become
enclosed at the metamorphosis and degenerate inside the epidermis. The only
difference between the two groups seems to be the degree of packing of the elements
within the cavity lined by the ectoderm.
The "coelom" of the ectoprocts clearly has the function of a "fluid skeleton"
(Clark, 1964). Strong muscles retract the polypide into the cystid and the contrac-
318 CLAUS NIELSEN
tion of muscles associated with the wall ofthe cystid tends to compress the body
cavity, thus causing the protrusion of the lophophore. The very same construction
is, however, found in the entoproct larva, in which the hyposphere can be retracted
into the episphere by some muscles between the episphere and the hyposphere. The
muscle system responsible for the expansion of the hyposph ere is not very strongly
developed but can easily be recognized, for example, in the larva of Loxosoma
pectinaricola.
A "fluid skeleton" has probably evolved independently in several systematic
groups (Clark, 1964, p. 216), and from the present knowledge of morphology and
development of the entoprocts and ectoprocts it seems reasonable to interpret the
body cavity of the ectoprocts as a specialized larval pseudocoele. This specialization
has taken place in connection with the evolution of the mechanism for retraction
of the large lophophore and has involved an enlargement of the body cavity and
the development of the muscles of the cystid.
It may be mentioned that several authors describe the coelom of the Phylacto-
laemata as being divided into three portions and take this as an indication of a
close relationship between this group and the Phoronida. Brien (1960) has, how-
ever, given a clear description of the "coelom" of the phylactolaemates and con-
cluded that the cavities of the epistome and the lophophore are continuous with
the general body cavity. He furthermore states that the only histological difference
between these regions lies in their ciliation. It appears that these facts do not give
any firm support to the theory that the ectoprocts should be derived from Phoro-
nis-like ancestors.
Muscles
The musculature of the Entoprocta is only poorly known. Cori (1936) pictures
some important muscles of the calyx of Pedicellina, but it is in several cases impos-
sible to see where the muscles attach. There is a longitudinal muscle at the frontal
side of each tentacle and a sphincter around the atrium at the base of the tentacles.
A number of ring-muscles are found around the oesophagus and some muscles
apparently originating at the atrium insert on the posterior side of the oesophagus
and may expand it. Some fibres apparently pull the posterior lip backwards over
the atrium. The rest of the digestive tract is devoid of muscles except for a constric-
tor between the intestine and the rectum and a constrictor of the anus. Strong
muscles retract the atrium when the animal becomes irritated; these muscles con-
tinue into the stalk in the loxosomatids, while the muscles of the calyx and the
stalk in the pedicellinids are separate and attach to the chitinous diaphragm at the
top of the stalk (see, e. g., Franzen, 1970b).
The Ectoprocta have a more differentiated system of muscles (Brien, 1960).
The tentacles have longitudinal muscles both along the frontal and abfrontal sides.
The whole alimentary canal possesses ring muscles, and in the Eurystomata and
Cyclostomata longitudinal muscles are also found. Bullivant & BiIs (1968) described
radiating striated muscle fibres in the epithelial cells of the oesophagus of

Zoobotryon (Eurystomata). A number of small muscles between the outer side of
the tentacle bases and the mouth may open the mouth. The polypide may become
retracted into the cystid by means of a pair of large muscles originating at the
basal part of the cystid and inserting on the basement membrane, which forms a
thickened ring at the base of the tentacles (Graupner, 1930; Nielsen, 1970). A
constrictor around the orifice is found in many species. The muscles of the cystid
wall which by their constriction make the polypide protrude, the parietal muscles,
spread over the cystid in the ctenostomes, while many elegant specializations are
found in the calcified species.
The body wall of the phylacto1aemates shows an outer layer of circular fibres
separated from an inner longitudinal layer by a thickened basement membrane

(Brien, 1953).
Various of the muscles, especially the retractors, have been described as striated,
but Brien (1960) has observed that the retractors in some of the phylacto1aemates
contain two (?) fibres which become helically coiled by the contraction. This
gives the cells a striated appearance, and the other "striated" muscles ought to be
studied more closely.
The present knowledge of the musculature in the two groups seems too in-
sufficient for a comparative discussion.
Ciliation and feeding mechanisms

Both entoprocts and ectoprocts are filter feeders.
In the Entoprocta the tentacles show an identical ciliation in all species in-
vestigated (Atkins, 1932b; Mariscal, 1965; Franzen, 1970b). The inner side of
each tentacle shows three rows of cells with short cilia (frontal cilia); the median
row is wide and slightly depressed and the lateral two are rather narrow. Lateral
to these cells is found a row of large lateral cells with a row of long syncilia. The
shapes of transverse sections vary between the species but the lateral cilia seem
always to originate just frontal to the widest part of the tentacle. The frontal
ciliary belts unite at the bases of the tentacles to form a horseshoe-shaped band
enclosing the mouth (adoral cilia) (see Fig. 80). The lateral row of synci1ia forms
a continuous band bordering the area of short cilia on all sides (see also Brien,
1960, and Fig. 77).
The beat of the lateral cilia creates a current between the tentacles directly
towards the centre of the lophophore, resulting in a strong current away from the
atrium (Fig. 80). At the same time these cilia catch particles from the water and
transfer them to the frontal cilia which carry the particles to the mouth (Atkins,
1932b).
Metachronal waves have not been observed in the movements of the lateral
cilia (Knight-Jones, 1954).
320 CLA us NIELSEN
Entoprocta Eurystomata Phylacto/aemata

+ Cyclostomata
Loxosome/la crassicauda Flustre/lidra hispida

FIG. 80. The ciliation and water currents of the lophophore of entoprocts and ectoprocts. Above,
the ciliation; the long cilia represent prototroch + metatroch, the dotted areas represent the
adoral ciliation; the mouth is black, and the anus is a circle. Below, cross sections of tentacle
crowns of an entoproct and an ectoproct, showing the water currents; after Atkins (1932b).
In the Ectoprocta (Fig. 80) the tentacles are usually widest near the outer
(abfrontal) side where a row oflarge syncilia is found (Borg, 1926; Atkins, 1932b;
Marcus, 1934; Lutaud, 1955). The frontal edges of the tentacles bear short cilia
which are only weakly developed or perhaps entirely lacking in some cyclostomes
(Borg, 1926).
The lateral cilia create a water current towards the mouth of the zooid and this
current becomes deflected over the mouth and flows between the tentacles (Fig.
80) (Atkins, 1932b; Bullivant, 1968). The mechanism employed to catch the par-
ticles has been described as impingement (Bullivant, 1968). This means that the
particles with higher specific gravity than the water become thrown against the
mouth (in the Cyclostomata and Eurystomata) or the ciliated groove between the
tentacles (in the Phylactolaemata) at the deflection of the current.
The role of the frontal cilia in feeding seems doubtful. Bullivant (1968) ob-
served particles being transported away from the mouth by the frontal cilia in
Plumatella repens. Borg (1926) and Atkins (1932b) observed a weak and probably
rather unimportant transport of particles towards the mouth by these cilia in some
cyclostomes and in Flustrellidra hispida, respectively.
The lateral cilia beat metachronally and the waves move clockwise when the
animal is seen from above (laeoplectic metachronism) (Knight-Jones, 1954).
The arrangement of the cilia is thus very similar in the two groups, and from
Fig. 80 it is clearly seen that the anus of the Entoprocta lies outside the ciliary
girdle just as it does in the Ectoprocta. The function is, however, quite different
and the gap between the two types seems difficult to bridge. A small hint may be
found in the observation by Bullivant (1968) that the lateral cilia of Zoobotryon
verticillatum may reverse their beat when larger particles become trapped by the
tentacles.
Alimentary canal
The histology and function of the V-shaped gut of the Entoprocta have been
studied by only few authors. Becker (1937) and Brien (1959) studied Pedicellina
cernua in detail; Atkins (1932a) studied Loxosomella obesa and Mariscal (1965)
gave some observations on Barentsia gracilis. The types studied show very similar
structures of the gut. All the epithelia are one-layered and ciliated.
The oesophagus is funnel-shaped, its posterior side being thickest and bearing
the heaviest ciliation. Becker (1937, p. 80) states that the oesophagus is not secre-
tory, but Brien (1959, p. 942) believes that this is where the mucus band which
carries the food particles through the stomach-intestine-rectum originates.
The stomach shows areas of different cell types. An area adjacent to the oeso-
phagus bears long cilia which are believed to rotate the mucus band through the
gut. The "roof" of the stomach is usually brownish in the live animals, and the
cells contain the brown material in a distal vacuole. Emschermann (1965b) ob-
served that various vital dyes became concentrated in these cells and were discar-
ded together with the distal tips of the cells. A glandular area occupying the poste-
rior part of the bottom of the stomach and part of its sides contains two types of
cells: one type which appears to secrete the digestive enzymes and the other which
is probably absorptive. Mariscal (1965) found that the "rod border" of these cells
is a dense layer of microvilli.
The intestine has a strong ciliation and is probably resorptive.
The rectum is sometimes brownish like the roof of the stomach and probably
has an excretory function.
The gut of the Ectoprocta is likewise U'-shaped and consists of a one-layered
epithelium. Important studies are those of Becker (1937), Silen (1944d) and Brien
21
322 CLAUS NIELSEN
(l960); a short review is given by Ryland (l970). The anterior part of the gut has
a ciliated upper region usually called the pharynx, and a non-ciliated lower region,
the oesophagus. The stomach comprises a descending tubular part, the cardia, a
central part with the caecum, and an ascending conical part, the pylorus. The lower
part of the cardia is specialized as a gizzard in some species. The cardia and the
stomach are devoid of cilia. In the Eurystomata and the Cyclostomata the pylorus
carries cilia, but these are lacking in the Phylactolaemata. The posterior thin-
walled non-ciliated part of the gut is either called intestine or rectum, 'but some
authors (e. g., Brien, 1960) distinguish two regions.
The food passes rapidly through the pharynx, which by Becker (l937) is con-
sidered secretory. In the Eurystomata and Cyclostomata the gut content rotates
as a rod-like body, probably kept together by a secretion (Silen, 1944d). In the

Phylactolaemata the food is pumped to and fro between the cardia and the cae-
cum by way of the musculature; according to Marcus (1934) and Becker (1937) it
is surrounded by a peritrophic membrane. The epithelium of the central part of
the stomach and the caecum consists of two types of cells: transparent uncoloured
cells which appear to secrete the digestive enzymes, and opaque brownish cells
which are probably resorptive. In the phylactolaemates the two cell types form
longitudinal bands. The particles giving the colour to the brownish cells are pro-
bably accumulated excretory products and these cells thus function as a "storage
kidney". At the degeneration of the polypide these particles give colour to the
"brown body" which in some cases becomes enclosed in the stomach of the re-
generated polypide and expelled through its anus. The rectum is probably both
resorptive and secretory. It appears from the above that the digestion is mainly
extracellular, but Marcus (l94l a) pictured diatoms inside some of the cells of the
caecum in Thalamoporella.
The digestive tracts of animals with similar feeding types usually contain the
same cell types. It is, therefore, not unexpected that important differences between
the digestion in the Entoprocta and the Ectoprocta have not been found, but
further investigations are needed before a detailed discussion can be carried out.
Nephridia
Allmost all loxosomatids and pedicellinids studied so far possess one pair of
protonephridia. In the loxosomatids they open separately in the atrium near
the ganglion (Harmer, 1885; Prouho, 1891, Gruijs-Faucher, 1959), but in the
pedicellinids there is an unpaired pore just in front of the ganglion (Stiasny, 1905;
Cori, 1936).
In Urnatella gracilis (studied by Emschermann, 1965b) a number of flame
cells are found on both sides of the calyx, all communicating with a pair of Y-
shaped terminal ducts which open through the common nephridiopore; additional
single protonephridia occur in the stalk where they open beneath the "spongy"
cuticle. The protonephridia develop from a single ectodermal cell which divides
to form the whole branched system with the terminal flame cells. Emschermann's
thorough study also showed that the function of the protonephridia is osmoregu-
latory, while excretion of various vital dyes takes place exclusively through the
cells of the stomach roof.
Electron microscopical studies on the two protonephridia of Pedicellina cernua
and the branched protonephridial system in the calyx of Urnatella gracilis have
been carried out by Brandenburg (1966) and Kiimmel (1962), respectively. Both
species show a fenestrated area at the basal part of the nephridial canal and are
thus examples of the cell type called cyrtocytes. Brandenburg (op. cit.) made a
comparison of the cyrtocytes of a number of systematic groups (Turbellaria,
Trematoda, Gastrotricha, Rotatoria, Polychaeta, Gastropoda, Lamellibranchia,

Entoprocta, Priapulida, and Acrania), but it seems premature to draw any phy-
logenetic conclusions on basis of the present knowledge which is based on investi-
gations on a few species within the groups mentioned.
The larvae of the pedicellinids and some of the loxosomatids have a pair of
flame cells which open lateral to the foot. They degenerate at the metamorphosis.
The ectoprocts have no nephridia. The ciliated funnels described as a sort of
metanephridia in the phylactolaemates are merely specially ciliated parts of the
common body cavity (Brien, 1960, p. 1086).
That the Entoprocta possess typical protonephridia while the Ectoprocta
totally lack nephridia seems of little value for phylogenetic considerations.
Nervous system
The nervous system of the Entoprocta comprises a compact ganglion in the loop
of the digestive tract and peripheral nerves to the tentacles and the stalk (Cori,
1936; Brien, 1959). The ganglion originates as a thickening of the ectoderm of the
atrium. It is usually hourglass-shaped, but Cori (1936) described it as ellipsoidal
in Pedicellina cernua. The nuclei are situated peripherally and usually are concen-
trated in the lateral parts. A concentration of fibres is found in the centre.
The peripheral nerves have been investigated, especially by Harmer (1885:
Loxosomella crassicauda) and Cori (1936: Pedicellina cernua) but several details
are still unclear and a more thorough study is strongly needed.
Some nerves from the lateral parts of the ganglion proceed to the lophophore
where a small ganglion is found at the base of each tentacle. Unicellular sense or-
gans at the tentacles, each with a sensory bristle, are connected with these ganglia
while similar sense organs on the calyx connect directly with the basal part of the
nerves from the central ganglion. One pair of nerves proceeds to the stalk. Hilton
(1923) found a net of nerve cells in the muscular base of the stalk of Barentsia
gracilis. A similar system was observed in the stolons where "sense pits" were also
said to occur.
2[0
324 CLAUS NIELSEN
The Eurystomata possess a small compact ovoid ganglion which lies at the
anal side of the mouth. It originates as an invagination from the ectoderm of the
region of the lophophore. Graupner (1930) found that the ganglion contained
about 25 nuclei embedded in a striated mass.
The peripheral system has been studied by Marcus (1926a), Graupner (1930),
Bronstein (1937), Brien (1960), and Lutaud (1969). Most conspicuous is the ring
nerve (ganglion), which lies above the ganglion and surrounds the oesophagus
almost completely; in the region below the abanal tentacles it is either interrupted
or very thin and without nuclei. This nerve (ganglion) contains many nuclei,
especially in the anal and lateral parts, and sends small sensory and motor fibres
to the tentacles. A pair of nerves leads from the ganglion to the tentacle sheath
and another pair follows the retractors of the polypide. A subepithelial network
is present in the cystid of Farrel/a; it is probably continuous with the nerves of the
tentacle sheath (Marcus, 1926a). In Electra three pairs of nerves run from the
ganglion along the tentacle sheath to the cystid wall; one innervates the parietal
muscles while the other two continue in a delicate ring of fibres along the basal
parts of the lateral walls of the cystid. These nerves continue through the pores
between the zooids and thus form a genuine colonial nervous system (Lutaud,
1969).
The nervous system of the Cyclostomata is very poorly described. There is a
ganglion which is very similar to that of the eurystomes both with respect to mor-
phology and development.
The Phylactolaemata have a nervous system which resembles that of the eU J
rystomes (Gerwerzhagen, 1913; Marcus, 1934; Brien, 1960). The modifications

shown in the phylactolaemates appear to be connected with the enlargement of
the lophophore and its altered shape. The ganglion, which is formed in the same
way as in the other ectoprocts, is hollow and has three strongly thickened areas
which protrude into its lumen while the portion closest to the anus consists of a
very thin epithelium. A pair of hollow protrusions (the ganglionic horns) follows
the two lophophore arms. The innervation of the tentacles, the gut and the cystid
is very similar to that of the eurystomes, as exemplified by Farrel/a.
The nervous systems of the Entoprocta and the Ectoprocta are thus very simi-
lar. The invagination to form the ganglion originates at the mouth region in the
ectoprocts and about halfway between mouth and anus in the entoprocts, but this
difference seems of minor importance. The small ganglia at the bases of the ten-
tacles in the entoprocts probably correspond to the compact nervous "ring" in
the eurystomes. In the phylactolaemates this ring has become modified further in
connection with the specialized tentacle arrangement.
Reproductive organs
The Entoprocta are probably all hermaphrodites, but most species are protandric
and this may be the reason why several species have been described as dioecious.
The loxosomatids usually have only one type of gonads at a time while both ovaries
and testes may be observed at the same time in some pedicellinids. The formation
of the gonads has only been studied by Hatschek (1877), who observed a pair of
large cells just above the stomach in the young buds. These two cells, which he
believed to be mesodermal, were surrounded by a very thin layer of cells. He
furthermore stated that the ovaries and testes develop from these cells and that
the gonoduct originates as an invagination from the atrial epithelium. Further
investigations seem to be needed to evaluate these findings and to elucidate the

earliest origin of the gonads.
The fully developed gonads are paired and sac-shaped and have a common
duct which opens in the posterior part of the atrium. The sacs consist of a one-
layered epithelium, from which the germ cells develop directly (Brien, 1959).
The eggs usually grow to a considerable size inside the ovaries. A number of
gland cells around the gonoduct secrete the membrane which surrounds the em-
bryos in most species.
In the male phase, the gonoduct of the loxosomatids is usually enlarged to
form a seminal vesicle.
The Ectoprocta have no well-defined gonads.
In the Eurystomata the germinal cells differentiate in groups from the lining
of the body cavity. The oogonia usually form one compact mass either on the
funiculus or on the basal part of the stomach, sometimes in the shape of a short
stalked sphere. The developing oogonia are surrounded by a thin epithelium (Prou-
ho, 1892). The ripe eggs float freely in the body cavity. In some species the fertilized
eggs start to develop in the body cavity and soon become enclosed in so-called
embryo sacs. In most cases, however, the eggs become expelled through a tempo-
rary pore between the anal pair of tentacles. This pore is in some species spe-
cialized as a ciliated funnel, the intertentacular organ. The spermatogonia develop
in several groups which are located either on the funiculus or on the cystid wall.
The zooids are hermaphroditic in most species and the male cells usually develop
before the female ones (Silen, 1966). In some cheilostomatous genera such as
Carbasea, Thalamoporella, Synnotum, Hippothoa, and Hippopodinella male and
female zooids can be distinguished within the hermaphroditic colonies (Stach,
1938; Marcus, 1938, 1941a, b; Rogick, 1956b; Gordon, 1968).
In the Cyclostomata the primary germinal cells with specially large nuclei
can be recognized at the growing edge of the colonies (Robertson, 1903). The
oogonia develop in the specialized gonozooids. The spermatogonia develop in the
funicular tissue at the lowermost part of the stomach of the autozooids.
326 CLAUS NIELSEN
In the Phylactolaemata the spermatogonia develop in clusters directly from

the cells of the funiculus, or as in Cristatella from the inner epithelium of the im-
perfect partitions between the zooids. The oogonia develop from the lining of the
body cavity just in front of a polypide. They become fertilized and migrate into
an embryo sac.
The important differences between the reproductive organs of the Entoprocta
and the Ectoprocta must be considered in connection with the development of a
spacious body cavity in the Ectoprocta.
Spermatozoa
The spermiogenesis of both Entoprocta and Ectoprocta has recently been reviewed
by Franzen (1956, 1970a). The spermatozoa of both groups are of a modified
type with strongly elongated heads, but considerable differences exist, especially
between the three ectoproct groups.
In the Entoprocta the spermatogonia differentiate in the sac-shaped testes.
The young spermatids are rounded and contain a large number of grain-like
mitochondria which aggregate to form first four and later on only two large
spheres at one side of the spherical nucleus, and a flagellum develops from this
region (Fig. 81 A-B). The mitochondrial spheres elongate and stretch along the
flagellum. The nucleus also elongates strongly and a small residual mass of cyto-
plasm becomes shed from the anterior part (Fig. 81 C-D). The mature spermato-
zoon (Fig. 81 E) is filiform with a head and a middle piece of about equal dimen-
sions; a ring-shaped centriole is found at the base of the head; the tail is about as
long as the middle piece and has a very thin sheath of cytoplasm.
The spermiogenesis of the Eurystornata follows a uniform pattern, but smal-
ler specific differences are found. The spermatogonia differentiate from the lining
of the body cavity and form groups which sometimes come to lie loose in the
cavity. During the following development the spermatids are attached to a common
cytoplasmic mass, the cytophore. At an early stage of the spermiogenesis the
mitochondria concentrate into two or four spheres which lie at the basis of a
developing flagellum (Fig. 81 F). The chromatin of the nucleus concentrates into
a conical body which gradually becomes long and slender. As the last phase of
the maturation the cytoplasm with the mitochondrial masses moves along the
flagellum, depositing its material (Fig. 81 G). The mature spermatozoon (Fig.
81H-N) which breaks off from the cytophore has a slender, sometimes lancet-
shaped head and a middle piece in which two bands of mitochondrial material
can be recognized more or less easily; the tail is rather short, lancet-shaped in
some species, filiform in others. Ring centrioles may be present at one or both ends
of the middle piece.
In the Cyclostomata the spermatogonia develop at the lower end of the sto-
mach. The four nuclei resulting from the meiotic divisions remain within a com-
H
10fJ
FIG. 81. Spermiogenesis and spermatozoa of entoprocts (A-E) and eurystomes (F-N). A-E, sper-
miogenesis and mature spermatozoon of Loxosoma rhodinicola; F-H, spermiogenesis and mature
spermatozoon of Flustra foliacea; I-N, mature spermatozoa of Caberea ellisi, Cryptosula palla-
siana ciliata, Monobryozoon limicola, and Bowerbankia sp. to show the variation within the eury-
stomes. A-K, N after Franzen (1956), L, M after Franzen (1970a). (Dr. Franzen has kindly in-
formed me that the species treated by him in 1956 under the name Loxosoma annelidicola is in
fact L. rhodinicola.i c, centriole; m, mitochondria.
328 CLAUS NIELSEN
FIG. 82. Spermiogenesis and spermatozoa of cyclostomes (A-F) and phylaetolaemates (G-K).
A-E, spermiogenesis and mature spermatozoon of Tubulipora liliacea; F, mature spermatozoon
of Diplosolen obelia; G-K, spermiogenesis and mature spermatozoon of Plumatella fungosa. A-F
after Franzen (1956), G-K after Franzen (1970a). c, centriole; m, mitochondria.
mon cytoplasm from which four flagella soon grow out. The mitochondrial ma-
terial concentrates into four small spheres at the base of each flagellum (Fig. 82A).
The nuclei become conical, with the chromatin arranged peripherally, and the
mitochondrial material arranges ina layer around the proximal parts of the
flagella, inside the common cytoplasm (Fig. 82B-C). Finally, some of the cyto-
plasm slides along the tails (Fig. 82D) and the mature spermatozoa (Fig. 82 E-F)
separate from a residual mass of cytoplasm. A ring centriole occurs at the anterior
end of the middle piece and in some cases a ring centriole is also found at its
posterior end.
The spermatogonia of the Phylactolaemata occur on the funiculus. The sper-
matids remain attached to a cytophore during almost the whole development.
The flagellum grows out from the cytoplasm, carrying an elongated mass of
cytoplasm at its distal part (Fig. 82 G). The mitochondria collect around the base
of the flagellum and form a cylindrical mass which later on elongates and slides
along the proximal part of the flagellum (Fig. 82I). The head of the spermatozoon
is small and pointed and the mitochondrial material forms a helix in the middle
piece (Fig. 82K).
There is thus much similarity between the spermiogenesis and spermatozoa
of the Entoprocta and the Eurystomata, whereas especially the type represented
by the Phylactolaemata appears to be more specialized. The type of sperm found
in the Entoprocta and Eurystomata is widely distributed among the "Protostomia"
(see Franzen, 1970a).
Budding and total regeneration

The budding of the Entoprocta is well investigated and has been described earlier
(pp 276-277). That of the Ectoprocta, however, is rather poorly known (see pp
305-306) and it is therefore only possible to compare the overall patterns. The
whole epithelium of the alimentary canal is formed from an invagination of the
body wall in the Entoprocta, and this is also the case in most of the Ectoprocta.
The ganglion is formed as a small invagination from the ectoderm between the
mouth and the anus in the Entoprocta and as an invagination from the mouth
region in the Ectoprocta. This difference does not seem to be important.
The zooids of the colonies are very incompletely separated from each other
in the phylactolaemates whereas complete walls only pierced by rather narrow
pores are found in the eurystomes, cyclostomes and entoprocts. The partitions
develop in all groups as infoldings from the body wall.
The polypides of the Ectoprocta have a limited existence (Hyman, 1959). One
or two months after their formation they retract permanently and start to degen-
erate, forming the so-called brown bodies. In the phylactolaemates these soon
break up into fragments whereas they form well-defined ovoid bodies in the other
groups. In some of the eurystomes the brown body becomes enclosed by the re-
generating polypide and expelled through the anus. In other eurystomes and in
330 CLAUS NIELSEN
the cyclostomes the brown bodies accumulate in the basal parts of the zooids.
When a brown body has been formed in a cystid a new polypide buds off from the
body wall in the usual way. In some of the stoloniferous ctenostomes (Triticella)
the whole "head" of the zooid detaches from the tip of the stalk, where a new
head regenerates (Sars, 1874).
The Entoprocta do not form any brown bodies, but the "heads" are occasion-
ally cast off by the colonies of the pedicellinids. New heads then develop from the
tips of the stalk (Reid, 1845; Nasonov, 1926), just as in Triticella.
Resting bodies (hibernaculae)

Thick-walled cysts which seem well fitted to endure unfavorable conditions have
been described in some species of the colonial Entoprocta.
The best known resting bodies are those of Barentsia matsushimana, described
by Toriumi (1951) and Emschermann (1961, as B. gracilis) (see also Franzen,
1970b). They are elongated bodies attached to the substratum with one side and
consist of a row of chambers filled with cells rich in a yolk-like material. They
have a thick cuticle and are usually formed at the tip of a short lateral stolon.
One-chambered resting bodies occur in B. kovalevskii (Valkanov, 1951, as
Arthropodaria kovalevskii] and Loxosomatoides japonicum (Toriumi, 1951). The
lemon-shaped cyst of Barentsia kovalevskii is formed at the tip of a stolon; at
the top it has a small pore through the thicker inner layer of the cuticle with a
plug of cells with large nuclei below. The stalk of a new polypide was observed to
develop through this pore.
Urnatella gracilis does not produce special resting bodies but the stalk with the
thick cuticle and numerous yolk-like inclusions overwinters without heads; single
joints of the stalk are also said to function as a sort of statoblast (Prenant & Babin,
1956; Wiebach, 1959).
New polyps appear to develop from the resting bodies through a budding
process which is quite identical to the normal budding and to the regeneration of
a new calyx from the tip of a stalk.
Thick-walled cysts have also been described in some eurystomes, especially
in species living in brackish or fresh water.
The distal parts of the colonies of some species die off in the winter and only
the basal parts of the colony survive and start a new colony in the spring. In Bugu-
la neritina, Numakunai (1960, 1967) observed that a number of buds develop from
the overwintering thick-walled basal stolons. He also observed that buds can de-
velop from cellular material squeezed out of these stolons. In such cases it appeared
that the cells after about one day had rearranged so that a thin "ectodermal"
layer could be distinguished surrounding an inner mass of cells more rich in a
yolk-like material. After five to six days the epithelium became columnar in some
places, forming weak protrusions, and soon after normal septa developed from
the peripheries of these areas. The polypides developed in the same way as the
normal polypide buds. Budding from overwintering stolons has also been observed
in Zoobotryon verticillatum by Zirpolo (1933).
Small thick-walled cysts of more irregular shapes develop from the stolons
in a couple of species such as Victorella pavida, V. muelleri, Bowerbankia caudata
(Braem, 1951), and Paludicella articulata (Kraepelin, 1887; Braem, 1914). Poly-
pides bud from these cysts in the same way as the normal polypide buds.
Dormant, closed zooids corresponding to the cysts have been observed in
Conopeum seurati (Hastings, in Ryland, 1970).
Special resting buds have not been described in the Cyclostomata, but Harmer
(1891) observed that single degenerating zooids of Crisia ramosa under certain
circumstances became closed by a calcareous diaphragm. Later on a new polypide

developed below the diaphragm, which then dissolved.
The Phylactolaemata produce the well-known resting bodies called statoblasts.
Their origin and whole morphology have been described in detail by several authors
and extensively summarized by Brien (1953, 1960) and Hyman (1959).
The statoblasts originate in the funiculus in zooids which have gone through
a phase of sexual reproduction. A small compact mass of ectodermal cells prolifer-
ates into the basal part of the funiculus where small spheres bud off one after the
other. The oldest statoblasts are accordingly found closest to the polypide and the
youngest ones closest to the base of the funiculus. The small sphere grows and
becomes hollow, and after some time it becomes flattened. The young statoblast
now forms a bulge on the funiculus covered by the funicular epithelium. Between
the flattened vesicle and the central layer of the funiculus a mass of cells rich in
"yolk" granules has formed a compact mass; these cells originate from the epi-
thelium of the funiculus. The flattened vesicle invaginates and soon surrounds the
mass of yolk-rich cells completely. Its outer cell layer becomes columnar and
secretes from its inner side the often very complicated chitinous valves of the sta-
toblast.
When the statoblast germinates after a resting period, the polypides develop
from the inner epithelial layer just below the valves. This budding takes place in
exactly the same way as the usual colonial budding.
At first sight the statoblasts of the phylactolaemates seem very different from
the resting bodies of the eurystomes. It appears, however, that the two types
consist of the same elements: An internal mass of cells, rich in yolk and origina-
ting from the mesoderm, surrounded by a layer of cells from the ectoderm; the
chitinous cuticle is secreted from ectodermal cells, the only difference being that
the cuticle of the statoblasts is secreted not from the ectoderm of the cystid but
from an extension of this epithelium.
The resting bodies of the Entoprocta and the Ectoprocta are thus directly com-
parable both with regard to development, morphology and germination. Similar
structures are, to my knowledge, known only from sponges and hydroids.
332 CLAUS NIELSEN
CONCLUSION
The above discussion has demonstrated significant similarities between the Ento-
procta and the Ectoprocta. Especially the larvae and their metamorphoses are
obviously comparable, and the same is true for the fundamental patterns of the
budding and the formation of the resting bodies. The most important difference
between the two groups is that a spacious body cavity is present in the Ectoprocta
but absent in the Entoprocta. It is, however, my opinion that the body cavity of
the Ectoprocta has evolved from the narrow spaces between the mesodermal
cells of the Entoprocta, in connection with the evolution of the retractible polypide.
A primitive "fluid skeleton" is present in the larva of the pedicellinids, and the
body cavity of the Ectoprocta clearly has the same function in connection with the
protrusion of the polypide. Real differences between the two groups seem to exist
only in the ciliary feeding mechanisms and perhaps in the cleavages.
The Entoprocta are definitely related to other groups having trochophore lar-
vae, but it is not possible to point to any group to which they show special affinities.
The consequence of these considerations is that the Entoprocta and the Ecto-
procta must be regarded as classes of a separate phylum, the Bryozoa.
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334 CLAUS NIELSEN
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338 CLAUS NIELSEN
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Entoproct life-cycles and the entoproct/ectoproct

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Abstract . . 210 Survey of entoproct life-cycles 271

have originated from buds, represents an intermediate type.

MATERIALS AND METHODS

gisk Laboratorium, Frederikshavn, Denmark; Kristinebergs zoologiska Station,

ENTOPROCT EMBRYOLOGY AND

Fam. LOXOSOMA TIDAE

Loxosomella atkinsae Bobin & Prenant, 1953

Loxosomella crassicauda (Salensky, 1877)

Loxosomella elegans Nielsen, 1964

FIG. 4. Loxosomella elegans. An almost median section of an expanded larva.

Loxosomella fauveli Bobin & Prenant, 1953

Loxosomella harmeri (Schultz, 1895)

FIG. 7. Loxosomella harmeri,

FIG. 8. Loxosomella harmeri.

stomach apical organ glandular cells above

rectum foot "sale" foot knob syncilium of the foot knob

FIG. 10. Loxosomella harmeri. A median section of an expanded larva.

O. F. Muller. The material treated below was collected in September-December

peri pedal groove foot "sole" prototroch

FIG. 16. Loxosomella harmeri. A median section of a contracted larva.

Loxosomella leptoclini (Harmer, 1885)

Loxosomella murmanica (Nil us, 1909)

already with small ciliated tentacle buds at its periphery.

Loxosomella neapolitana (Kowalewsky, 1866)

Loxosomella obesa (Atkins, 1932)

Loxosomella pes (Schmidt, 1878)

Loxosomella phascolosomata (Vof?;t, 1876)

Loxosomella polita Nielsen, 1964

Loxosomella scaura Nielsen, 1964

Loxosomella tethyae (Salensky, 1877)

Loxosomella varians Nielsen, 1964

Loxosomella vivipara Nielsen, 1966

Loxosoma davenporti Nickerson, 1898

NEW OBSERVATIONS: A few of the specimens mentioned in an earlier paper (Niel-

ing of the epithelium resembling early stages of buds.

Loxosoma jaegersteni Nielsen, 1966

Loxosoma okudai Yamada, 1956

Loxosoma pectinaricola Franzen, 1962

NEW OBSERVATIONS: This species is very common on the pectinariid polychaete

lateral sense organ

prototroch constrictor oesophagus ffitractor prototroch nerve

stomach frontal ganglion

to lateral sense orqan

oesophagus retractor nerve to prototroch small muscles from epi- to hyposphere

outer lateral lateral groove stomach stalked vesicle

prototroch constrictor oesophagus

muscles from prototroch cells

Loxosoma rhodinicola Franzen, 1962

NEW OBSERVATIONS: Many adult specimens attached to the maldanid polychaete

and Fiskebackskil (Swedish west coast), depth about 50 metres, in August-Sep-

Pedicellina cernua (Pallas, 1774)

FIG. 34. Pedicellina cernua. A median section of an expanded larva.

FIG. 35. Pedicellina cernua. A median section of a strongly contracted larva.

FIG. 36. Pedicellina cernua. A median section of a newly settled larva.

FIG. 37. Pedicellina cernua. A newly settled

larva; a protonephridium and five cells con-