HELGOLANDER MEERESUNTERSUCHUNGEN
Helgol~nder Meeresunters. 44,425-444 (1990)
Post-embryonic larval development and metamorphosis
of the hydroid E u d e n d r i u m r a c e m o s u m (Cavolini)
(Hydrozoa, Cnidaria)
C. S o m m e r
Lehrstuhl ffir Spezielle Zoologie und Parasitologie,
Ruhr-Universit~t Bochum; D-W-4630 Bochum, G e r m a n y
ABSTRACT: The morphology and histology of the planula larva of Eudendriurn racemosum
(Cavolini)' and its metamorphosis into the primary polyp are described from light microscopic
observations. The planula hatches as a differentiated gastrtfla. During the lecithotrophic larval
period, large ectodermal mucous cells, embedded between epithellomuscular cells, secrete a sticky
slime. Two granulated cell types occur in the ectoderm that are interpreted as secretory and sensorynervous cells, but might also be representatives of only one cell type with a multiple function. The
entoderm consists of yolk-storing gastrodermal cells, digestive gland cells, interstitial cells, cnidoblasts, and premature cnidocytes. The larva starts metamorphosis by affixing its blunt aboral pole to
a substratum. While the planula flattens down, the mucous cells penetrate the mesolamella and
migrate through the entoderm into the gastral cavity where they are lysed. Subsequently, interstitial
cells, cnidoblasts, and premature cnidocytes migrate in the opposite direction, i.e. from entoderm to
ectoderm. Then, the polypoid body organization, comprising head (hydranth), stem and foot, all
covered by pefidermal secretion, becomes recognisable. An oral constriction divides the hypostomal
portion of the gastral cavity from the stomachic portion. Within the hypostomal entoderm, cells
containing secretory granules differentiate. Following growth and the multiplicationof tentacles, the
head pefiderm disappears. A ring of gland cells differentiates at the hydranth's base. The positioning of cnidae in the tentacle ectoderm, penetration of the mouth opening and the multiplication of
digestive gland cells enable the polyp to change from ledthotrophic to planktotrophic nutrition.
INTRODUCTION
Life cycle i n the E u d e n d r i i d a e comprises the typical cnidarian larva, the planula,
which metamorphoses into a primary polyp that by asexual reproduction gives origin to a
m o n o p o d i a l l y - g r o w i n g colony (K/ihn, 1913; Mergner, 1957). Due to complete suppression of the m e d u s a g e n e r a t i o n in all m e m b e r s of the family, gonadial tissue is b o r n e on
specialized male a n d female hydranths, n a m e d blastostyles. The source a n d m a t u r a t i o n
of oocytes as well as the embryonic d e v e l o p m e n t of p l a n u l a e were thoroughly a n a l y s e d
by M e r g n e r (1957) i n Eudendrium racemosum a n d b y Wasserthal (1973) in E. armature.
Hanisch (1966, 1970) investigated spermatogenesis in E. racemosum.
In contrast, the post-embryonic period, i n c l u d i n g larval d e v e l o p m e n t , settlement,
a n d metamorphosis, has still received little attention. Some information o n the larval
biology of E. armature, E. rameum, a n d E. racemosum, especially c o n c e r n i n g the vivid
m u c u s secretion of floating p l a n u l a e a n d its ecological importance, was g i v e n b y
9 Biologische Anstalt Helgoland, Hamburg
426
C. Sommer
Wasserthai & Wasserthal (1973). The only histological description of metamorphosis in
the Eudendriidae is a brief note on E. racemosum published by Mergner (1971) as part of
a general survey on developmental biology in the Cnidaria. He reported the disappearance of mucous and sensory-nervous cells from the ectoderm and the migration of
interstitial cells, cnidoblasts, and premature cnidocytes from entodermal to ectodermal
germ layer shortly after the onset of metamorphosis.
Histological data on larvae and their metamorphosis are available from several other
hydroid families, e.g. Clavidae (Morgenstern, 1901; Harm, 1903; van de Vyver, 1967),
Hydractiniidae (van de Vyver, 1964, 1967; Bodo & Bouillon, 1968; Weis et al., 1985; Weis
& Buss, 1987), Corynidae (van de Vyver, 1967; Bodo & Bouillon, 1968), Halocordylidae
(Hargitt, 1900; Martin & Thomas, 1977, 1980, 1981a, b; Hotchkiss et ai., 1984; Martin &
Archer, 1986a, b), and Mitrocomidae (Martin et al., 1983). They indicate a mixture of both
constant and variable developmental patterns between different families, revealing
hydroid metamorphosis as a profitable field for comparative developmental studies.
M A T E R I A L AND METHODS
Female colonies of Eudendriurn racemosum {Cavolini) bearing numerous developing
embryos were collected during August/September 1986 by SCUBA- or skin-diving along
the coast of the Portofino Peninsula, about 30 km southeast of Genoa, Italy, at depths from
0.5 to 25 m. The colonies were kept for up to two weeks at 22-26 ~ in round plastic bowls
containing daily-changed, filtered sea water (ca 2 cm depth), without feeding or aeration.
Hatched planulae were harvested twice a day and transferred with a pipette to petri
dishes. Larval settlement and metamorphosis were easily induced by adding pieces of
marine algae such as Ulva lactuca and Enteromorpha sp. or other natural substrata taken
from the sea. Free planulae or specimens at selected s~ages of metamorphosis were fixed
in Bouin's fluid, 4 % formaldehyde, or picro-formol (after Jha, 1965), at room temperature
overnight, and then transferred to 70 % ethanol. Following dehydration they were
embedded in Paraplast-Plus, cut to 5 ~m sections and stained with azan (after Heidenhain), azure II - eosine (after Nocht-Maximow), Giemsa's solution, iron hematoxyline
(after Weigert or Heidenhain), or acid hemalum (after P. Mayer or Ehrlich) (details after
Romeis, 1968, and Burck, 1973). The best results were obtained with azan. This stain was
sometimes combined with alcian blue 8 GS, a selective dye for acid mucopolysaccharides
(Chayen et al., 1975).
The histological illustrations were drawn with the aid of a drawing tube (Leitz)
mounted on a Leitz-Dialux light microscope, using bright field and phase-contrast
equipment alternately.
RESULTS
H a t c h i n g of p l a n u l a e
At the time of hatching, the larva has already attained the diploblastic body
organization peculiar to all Cnidaria, comprising an inner entoderm (Fig. 1; ent) and an
outer ectoderm (ect), separated by a thin, acellular sheet, the mesolamella (mes).
A peridermal envelope (Fig. 1; pe) surrounds the embryo from an early stage of
development (cf. Mergner, 1957), and hatching is initiated by a striking decrease in its
L a r v a l d e v e l o p m e n t a n d m e t a m o r p h o s i s of E u d e n d r i u m
racemosum
427
nC
....,~i~i~84
'i
: ::~24
9 i~.i
%~
~.~ "
,: /
~
9 " .
~
.~
.:.i.~
~!ii i~'~~i'
:~,4~~",.
e~, ~
3
9
\i
Figs 1-3. E u d e n d r i u m r a c e m o s u m . 1. Hatching planula; 2. Post-hatching larva; 3. Aboral pole of a
planula (only ectodermal layer drawn). Scales: Fig. 1:50 ~m; Fig. 2 : 1 0 0 ~m; Fig. 3 : 1 5 ~m
428
C. S o m m e r
thickness. This process culminates locally in the formation of a circular o p e n i n g at the
a n i m a l pole of the e g g capsule, w h i c h corresponds in position with the aboral p o l e of the
planula. At the opposite pole the e g g is f a s t e n e d to the f e m a l e blastostyle by a thick an d
m u l t i l a y e r e d p e r i d e r m socle (Fig. 1; ps).
Planulae always hatch by l e a v i n g the e g g aboral pole first. T h e n t h e y slowly w i n d
Abbreviations:
ad
annular depression
af
annular folds
as
algal substratum
bc
basophllic cells
cb
cnidoblast
c e n t cnidocytes remaining in the entoderm
cs
constriction
dgc digestive gland cell
ect
ectoderm
ent
entoderm
er cn erected cnidae
gc
gastral cavity
gcr
gland cell ring
gdc
gastrodermal cells
g
granula
grz
granular ring zone
hc
hypostomal cnidocyte
h ent hypostomal entoderm
hgc hypostomal granula cells
ic
i-cells
jc
junction canal
1
lacunae in the gastral cavity
m
mouth
mc
mucous cells
mes rnesolamella
n
nests of i-cells, cnidoblasts, and premature cnidocytes
nc
neck
nmb nucleus of a mucoblast
nmc nucleus of a mucous cell
np
nuclear particles of a mucous cell
p
periderm
pe
peridermal envelope
ph
pharynx
ps
peridermal socle
r
ring structure containing i-cells, cnidoblasts, and premature cnidocytes
rcl
reserve cells of type 1
rc2
reserve cells of type 2
rf
ring-furrow
sc
secretory cell
snct presumed sensory-nervous cell of type 1
snc2 presumed sensory-nervous cell of type 2
st
stolon
tac
tentacular axial cell
tb
tentacle buds
tgc
tentacular projection of the gastral cavity
vct
vitellophagous cells of type 1
vc2
vitellophagous cells of type 2
Larval development and metamorphosis of E u d e n d r i u m r a c e m o s u m
429
the hind part of their body through the opening in the egg membrane. Especially the
ectoderm of the larva becomes highly constricted as it passes through the narrow opening
{Fig. 1).
The most prominent elements in the ectoderm besides epithehomuscular cells are
mucous cells (Fig. 1; mc). They are mainly concentrated towards the aboral pole. Cells of
this type are swollen, often vase- or bottle-shaped and filled with an amorphous, lowrefringent, alcianophilic material. Observations on living animals demonstrated that
mucus secretion begins intensively even during the course of hatching. Thus, after
leaving the egg, the larvae stay in contact with the empty capsule for some time, still
attached by a slowly prolonging, sticky slime rope that extends from the oral pole of the
planula to the surface of the egg capsule. This behaviour, termed "roping down", has
been described in E. a n n a t u m , E. r a m e u m , and E. r a c e m o s u m (Wasserthal & Wasserthal,
1973).
A characteristic feature of the entoderrn is the high density of stored yolk particles.
After staining with azan, several types of yolk can be distinguished: (1) deep blue
particles of irregular shape; (2} a pale blue, probably more "hquid" mass not lying within
the gastrodermal cells but free in the developing gastral cavity; (3) blue particles similar
to those described under {1), but containing lots of red granules of differing grades of
density, and (4} pure red particles which are always spherical, but of varied sizes. Except
for type 2, yolk is normally enclosed in large gastrodermal cells which contain only small
amounts of cytoplasm.
In addition to yolk, the inner germ layer contains great numbers of non-differentiated
interstitial ceils (i-cells) together with cnidoblasts and premature cnidocytes. These are
concentrated in the mid-gastric region of the planula, most of them lying as clustered
nests near the mesolamella (Fig. 1; n). Digestive gland cells are rarely found (Pig. 5).
Free p l a n u l a e
Newly-hatched planulae are worm-shaped and about 0.6-0.7 mm long. The aboral
pole is blunt and the oral pole is tapered. After hatching, the body elongates and may
reach a length of 1.3-1.6 mm after one day. Free planulae are not able to swim actively
but float passively for some time, being distributed by currents. When eventually they
adhere to a substratum with the help of secreted mucus, the larvae ghde forward with the
aboral pole ahead. This movement is coupled with a slow anti-clockwise rotation of the
body. At the same time, a planula leaves a slime trail behind similar to that of a snail. The
forward-movement is produced by the beating of ectodermal cilia.
The cellular composition of the germ layers does not alter after hatching. Ectodermal
epithehomuscular cells are cyhndrical, with their nuclei being normally located in the
middle or apical region. Shortly behind the aboral pole, the epithehomuscular cells
possess a conspicuous apical granulation that forms a granular ring zone around the
larval body (Fig. 2; grz). In all planulae, mucous cells are concentrated at the aboral pole
and, to a lesser extent, at the tapered oral pole, but are also sparsely scattered over the
whole body (Fig. 2; mc).
Certain findings possibly indicate that the nuclei of older mucous cells degenerate by
fragmentation. Nuclei of younger cells (mucoblasts) are approximately spherical to
ellipsoid with diameters of about 8-10 ~tm, and possess a single, great nucleolus (Fig. 2;
430
C. Sommer
nmb). Maturation of the cells is accompanied by the condensation of chromatine, while
the shape of the nucleus becomes irregular due to the formation of protruding spines and
hooks (Fig. 2; nmc). Subsequently, some of the protrusions apparently break off and are
randomly dispersed in the surrouncling mucus. Fragmentation is continued until the
nucleus is totally degraded into small particles (Fig. 3; np), the fate of which cannot be
followed. Synchronously with nuclear degeneration, the amount of cytoplasm is more
and more diminished and replaced by mucus.
Two other ectodermal cell types are present in hatching as well as in free planulae.
They resemble each other in containing densely-packed, acidophihc granules and can be
distinguished only on the basis of cell morphology. The first type is similar to
epithehomuscular cells in being long and cylindrical (Fig. 2; sc). WasserthaI & Wasserthal
(1973) described cells hke these from mature planulae of E. a r m a t u m and supposed them
to be secretory in function ("kleine sekretorische Zellen", i.e. small secretory cells). The
second cell type differs from the first in having one or two long plasma processes running
from the cell's basal region between the intercellular spaces of neighbouring
epithehomuscular cells (Figs 2, 3, 4; sncl). Others project a very dehcate fibre apicad that
can ramify several times and probably ends free in the epithehum (Fig. 3~ snc2). Similar
cells have been well described and illustrated in the embryological study of Mergner
(1957) and were named "Sinnesnervenzellen" (i.e. sensory-nervous cells) to stress their
presumed dual function of stimulus perception and conduction.
The entodermal epithehum of a post-hatching planula centrally borders a lengthwise
extending gastral cavity (Fig. 2; gc). It widens near the aboral pole and narrows at the
oral one. The absence of a mouth and the presence of numerous yolk particles stored
within the low-columnar gastrodermal cells show the larva to be lecithotrophic.
In the majority of post-hatching planulae, the entodermal nests of i-cells, cnidoblasts,
and premature cnidocytes are not so concentrated as ir~ hatching ones, perhaps due to the
longitudinal extension of the planula body (see above}. A few i-cells and premature
cnidocytes penetrate the mesolamella and move into the ectoderm. However, no cnidae
are arranged in a position for discharge between the epitheliomuscular cells. Based upon
the typical stylet apparatus, all cnidocysts detected in both germ layers can be classified
as microbasic euryteles.
Digestive gland cells (zymogen cells) are comparatively scarce. Their number does
not exceed 12 per larva, most having about 8 (Fig. 17}. They have a slender, gobletshaped cell body (Fig. 5}, with the pointed base normally touching the mesolamella. The
apical portion of the cell is filled with a large quantity of acidophihc secretory droplets.
Characteristically, the nucleus contains a swollen nucleolus.
Metamorphosis
Within a period of 2.5 h to about 1 d after hatching, most of the planulae observed
attached to a substratum and began to metamorphose. Based upon morphological and
histological criteria, the transformation of the larva into a primary polyp can be subdivided into 9 stages. Metamorphosis is completed within 21-24 h.
S t a g e 1 : The larva attaches to the ground by its anterior (= aboral) pole and raises
the hind body slowly until it stands free in an upright position. Its initial adherence is
probably due to a sticky mucus secreted by the frontally-condensed mucous cells.
Larval d e v e l o p m e n t a n d metamorphosis of E u d e n d r i u m
racemosum
431
af,
i ~84184
ii~
aS
_. \
.....
~ ~ _
~.
6
sn~
Figs 4-8. E u d e n d r i u m r a c e m o s u m . 4. Oral pole of a planula (only ectodermal layer drawn); 5.
Digestive gland cell between entodermal cells; 6. Stage 1 of metamorphosis; 7. Stage 2 (early phase);
8, Stage 2 (late phase). Scales: Fig. 4:20 ~m; Fig. 5:10 ~m; Figs 6-8:50 ~m
432
C. S o m m e r
S u b s e q u e n t p e r m a n e n t fixing to the substratum is b y p e r i d e r m a l m a t e r i a l s e c r e t e d from
the e p i t h e h o m u s c u l a r cells. A l t h o u g h a secretion was n o t directly visible u n d e r the h g h t
microscope, this conclusion was d r a w n b e c a u s e of the s u d d e n loss of a p i c a l g r a n u l a from
the e p i t h e h o m u s c u l a r cells w h e n t h e y c a m e to a d h e r e to the substratum. T h e a d h e s i o n
zone e n l a r g e s continuously from a central, spot-like r e g i o n o u t w a r d s until it covers a
relatively wide, circular p l a n e on the u n d e r l y i n g surface (see Fig. 6).
T h e m u c o u s cells exhibit an i n c r e a s e d secretory activity d u r i n g p l a n u l a attachment,
b u t t h e y are n e v e r e m p t i e d completely. Those situated n e a r the a b o r a l p o l e b e c o m e
u n a v o i d a b l y e n c l o s e d b e t w e e n substratum, mesolamella, a n d the n e i g h b o u r i n g epidermal cells {Fig. 6; mc). This results in the termination of mucus secretion. The small
secretory a n d sensory-nervous cells l o c a t e d aborally b e c o m e e n c l o s e d too, b u t the
question of h o w their n o r m a l functions are affected b y this e v e n t cannot y e t b e a n s w e r e d .
The e n t o d e r m is not directly involved in the attachment. H o w e v e r , it t a k e s p a r t in the
c h a n g e s in proportion of the larval b o d y c o n n e c t e d with settlement. W h e r e a s the free
p l a n u l a is w o r m - h k e in shape, following settlement its anterior e n d swells considerably.
This is c a u s e d b y t h e progressive e n l a r g e m e n t of the a d h e s i v e region. A t this time, the icells, cnldoblasts, a n d p r e m a t u r e cnidocytes move forward a n d c o m e to he in the
e n t o d e r m a l wall of t h e t h i c k e n e d anterior portion of the b o d y (Fig. 6; n). Simultaneously,
the gastral cavity b e c o m e s b r o a d e r at the a d h e s i v e e n d b u t almost d i s a p p e a r s at the
opposite one, e x c e p t for some transiently persisting small l a c u n a e (Fig. 6; 1).
S t a g e 2 : T h e following s t a g e in d e v e l o p m e n t is c h a r a c t e r i z e d b y the l a r v a ' s
g r a d u a l s h o r t e n i n g in length. The b o d y flattens a n d the e n l a r g e m e n t of the a b o r a l
a d h e s i v e zone started in stage 1 continues {compare Fig. 7 with Fig. 8). A typical
associated feature is the formation of a n n u l a r folds or wrinkles r u n n i n g t h r o u g h the
e c t o d e r m (Fig. 7; af). T h e y m a y result from strong contractions of the myofibrils of the
e p i t h e h o m u s c u l a r cells.
At the b e g i n n i n g of stage 2, a v e r y thin p e r i d e r m l a m e l l a b e c o m e s visible b e t w e e n
the centre of the a d h e s i v e disk a n d the u n d e r l y i n g surface {Fig. 7; p). Its location
c o r r e s p o n d s to the spot-like region that w a s the first to stick to the s u b s t r a t u m d u r i n g
stage 1. T h e p e r i p h e r a l zone of the a d h e r i n g e c t o d e r m i n c l u d e s at l e a s t a major part, if
not all, of the g r a n u l a r ring zone that w a s d e s c r i b e d in the f r e e - h y i n g p l a n u l a .
During the flattening period, e c t o d e r m a l m u c o u s cells are f o u n d to cross the
m e s o l a m e l l a a n d to m i g r a t e i n w a r d s to the entoderm. This m o v e m e n t typically starts in
the a d h e s i v e r e g i o n (Fig. 7; mc). A short time later the first m u c o u s cells of the u p p e r
e c t o d e r m also start to i m m i g r a t e b y forcing their b a s a l e n d s t h r o u g h small o p e n i n g s in the
mesolamella. After the foot is a n c h o r e d b e t w e e n the b a s e s of g a s t r o d e r m a l cells, it swells
b y the influx of cellular contents from the e c t o d e r m a l side. Thus the v o l u m e still
r e m a i n i n g in the e c t o d e r m is progressively diminished. F i g u r e 7 shows t h r e e m u c o u s
cells of the u p p e r e c t o d e r m in an early to middle state of their p a s s a g e , a n d F i g u r e 8
shows four at a m i d d l e to late stage.
W h e n the m u c o u s cells h a v e i n t r u d e d into the e n t o d e r m , t h e y do not stay n e a r the
m e s o l a m e U a b u t continue their centripetal movement. P r o b a b l y d u e to t h e g r e a t n u m b e r
of i m m i g r a t e d cells, the volume of the i n n e r layer increases, resulting in a n i n c r e a s e in the
e p i t h e h a l thickness and, in parallel, a d e c r e a s e of the v o l u m e of the central gastral cavity
(Figs 7, 8; gc).
S t a g e 3 : The a t t a c h e d larva n o w has flattened to a m a x i m u m d e g r e e (Fig. 9). At
Larval development and metamorphosis of E u d e n d r i u m r a c e m o s u m
433
about the same time, the enlargement of the adhesive disk ceases. Thus, the formerly
worm-hke larval body is altered to a lens- or button-hke shape, with the adhesive zone
representing the aboral end of the planula.
The ectoderm is nearly free of mucous cells, and only the basal adhesive epithehum
may still contain some late-immigrating cells (Fig. 9~ mc). Those mucous cells that m o v e d
into the entoderm during stage 2 disappear from this tissue during stage 3. At the same
time, increasing amounts of acid mucopolysaccharides can be demonstrated in the
gastral cavity by the use of alcian blue or azure II. Hence, it is highly conclusive that
mucous cells are released into the gastric lumen following loss of their cellular boundaries.
Similar to the mucous cells, the small secretory and sensory-nervous cells described
in the planula throughout the ectoderm are not present any longer. A more detailed
information on their fate, however, could not be obtained.
While the migration of mucous cells from ectoderm to entoderm is almost completed,
i-cells, cnidoblasts, and premature cnidocytes begin to cross the mesolamella in the
opposite direction. The location of their passage is strictly confined to the base of the
button-shaped organism, slightly above the adhesive region. Here, the three cell types he
condensed on the entodermal side in a ring structure parallel with the plane of the
adhesive zone {Fig. 91 r}. Subsequent to their entry into the ectoderm the i-cells,
cnidoblasts, and premature cnidocytes move orally as well as aborally. However, they do
not invade "the basal adhesive epithehum. The premature cnidocytes spread over the
upper ectoderm more rapidly than do the i-cells and cnidoblasts.
During stage 3, a n e w cell type is generally noticed in small numbers. It is found
either located b e t w e e n the apices of the gastrodermal cells (Fig. 9~ vcl) or floating in the
gastral cavity {Fig. 91 vc2). All cells of this type have a v e r y l a r g e nucleus the diameter of
which ranges from 5.5 up to 10.5 ~tm. The nucleus is surrounded by yolk belonging to
type 2 (cf. section on "Hatching of planulae"). When the cell floats freely in the gastral
lumen, the yolk develops an acidophilic granulation. Gradually the yolk b e c o m e s mpre
and more reduced until there remains only a thin film surrounding the nucleus. Because
of these characteristics, the described cell type is regarded as a vitellophagous cell that
performs an accelerated yolk decomposition, compared with that of normal gastrodermal
cells.
Stages
4 a n d 5" A blunt-ending column grows up from the centre of the
flattened disk {Stage 4, Fig. 10). Following this, a shght constriction at the base of the
column and a w e a k swelling of its distal part divide the b o d y into 3 portions~ the upper
represents the future h e a d (= hydranth), the middle the stem, and the lower the foot of
the developing primary polyp {stage 5, Fig. 11).
The composition of the two germ layers differs from that of the planula due to the preceding outwandering of several cell types from their original epithehum (see description of
stages 2 and 3). The ectoderm now consists of epithehomuscular cells, i-cells, cnidoblasts,
and premature cnidocytes. The entoderm contains gastrodermal cells, digestive gland
cells, and a small n u m b e r of remaining premature cnidocytes {Figs 10, 111 c ent}.
At stage 4, the epithehomuscular cells of the upper side of the basal disk {foot}
produce a thin peridermal covering {Fig. 10~ p). The secretion of periderrn is continued
over the developing h e a d during stage 5 {Fig. 111 p}. Thus the organism is completely
surrounded by an acellular peridermal layer at the end of stage 5.
434
C. S o m m e r
~
~vc
~'
Figs 9-11.
Eudendrium
racemosum.
1
~
r
....
~
'~2. ~
9. Stage 3 of metamorphosis; 10, Stage 4; 11. Stage 5.
Scales: 50 ~m
Larval development and metamorphosis of
Eudendrium
racemosum
435
The oral projection of the gastral cavity widens considerably when the distal body
portion swells to form the primordial head (compare Fig. 10 with Fig. 11; gc). Synchronously, a distinct entodermal differentiation at the top of the head marks the initial
development of the hypostome (Fig. 11; h ent). The cells found here are lowered, closelypacked and cylindrical with small nuclei. Their plasma contains only very small amounts
of yolk, in contrast to other gastrodermal cells.
S t a g e 6 : This stage comprises two morphogenetic events: (1) The formation of an
annular constriction, separating an oral cap, the future hypostome, from the lower
hydranth body (Fig. 12; cs), and (2) the appearance of several vertical (i.e.longitudinal)
furrows that run through the hydranth wall and divide it into 6 or 7 tentacle buds. The
latter are hardly visible in longitudinal section but are well shown in transverse ones
(Fig. 13; tb). Figure 13 shows that both germ layers are involved in the formation of even
the youngest buds observed. Centrally, the buds consist of entodermal cells with strongly
basophilic cytoplasm and low yolk content (Fig. 13; bc). A short projection of the gastral
cavity runs into the base of every tentacle bud (Fig. 13; tgc).
The distribution of i-cells,cnidoblasts, and premature cnidocytes is not significantly
altered since they m o v e d into the ectodermal layer. Most of the i-cells and cnidoblasts are
found crowded in the upper basal disk, while premature cnidocytes are intermingled
with them as well as irregularly dispersed throughout the stem and the hydranth
ectoderm.
The differentiated entoderm of the developing hypostome has by this time enlarged
(Fig. 12; h ent). Its boundary with the typical yolk-containing gastrodermal cells of the
lower hydranth body corresponds to the external groove separating the hypostomal cap
from the tentacular region. D u e to the process of constriction, the gastral cavity becomes
parted into hypostomal and stomach portions. The junction canal between them is still
relatively wide at the developmental stage illustrated in Figure 12 (jc).
S t a g e 7 : Following the formation of the circle of 6 or 7 primordial tentacle buds
the bud tips start to grow in an oral direction. N e w buds originate one by one from the
same circle, raising the tentacle number to 9-13 at stage 7 (Fig. 18). Synchronously,
further constriction of the hypostomal base occurs.
The decomposition of yolk n o w becomes drastically enhanced in the gastral
epithelium of the basal disk, stem, and hydranth body. Most of the cells show a significant
decrease in the quantity of yolk granules, apparently accompanied by a slight increase in
the amount of cytoplasm. As a result, the gastrodermal cells shrink a little(Fig. 14; gdc).
T w o exceptions from this rule are generally noticed: (I) Between the numbers of cells
shrinking in the described manner, a few remain in the characteristic embryonic state,
that is with large cell bodies rich in yolk material, and are therefore called "reserve cells"
(Fig. 14; rcl). (2) Similar cells, though grouped instead of single, surround the junction
canal that links the hypostomal portion of the gastral cavity with the stomach (Fig. 14;
rc2).
S t a g e 8 : Morphologically, stage 8 is characterized by the further outgrowth of the
embryonic tentacles and the continuous formation of n e w ones. Their total number
reaches 11-17 (Fig. 18). In addition, the base of the hypostome n o w becomes fully
constricted, thus separating the oral (hypostomal) from the aboral (stomachic) gastral
lumen by a tightly-closing pharynx {Fig. 15; ph).
The peridermal sheet, wholly covering the ectoderm of the metamorphosing animal
436
C. S o m m e r
tb
~bc
Figs 12-14. E u d e n d r i u m r a c e m o s u m . 12. Stage 6 of metamorphosis; 13. Transversal section through
the tentacle b u d d i n g region at the level indicated by arrows in Fig. 12; 14. Stage 7. Note periderInal
covering over the head. Scales: 50 ~m
Larval d e v e l o p m e n t a n d m e t a m o r p h o s i s of
Fig. 15.
Eudendrium racemosum.
Eudendrium
racemosum
437
Stage 8 of metamor!~hosis. Scale: 100 ~m
since stage 5, b e c o m e s lost over the hypostome, the tentacles, a n d most of the b o d y wall
of the hydranth. It persists over the h y d r a n t h base, the stem, a n d the foot (Fig. 15; p). The
location of the u p p e r m a r g i n of the p e r i d e r m t u b e a l w a y s corresponds to a ring of
differentiating e c t o d e r m a l cells that are conspicuous b y their i n c r e a s i n g p l a s m a t i c
basophily, forming a g l a n d cell ring (Fig. 15; gcr). I m m e d i a t e l y a b o v e this structure, a
very slight a n n u l a r depression runs a r o u n d the surface of the e c t o d e r m (Fig. 15; ad).
P r e m a t u r e cnidocytes are now more frequently found in the t e n t a c u l a r e c t o d e r m
t h a n in the p r e c e d i n g stages. M o s t of the cnidae h e with their longitudinal axes almost
p a r a l l e l with the mesolamella, p r o b a b l y i n d i c a t i n g that t h e s e cells have not y e t finished
migration. Others have e r e c t e d their capsule so that its p o i n t e d e n d pierces the epithelial
surface (Fig. 15; er cn). These are t h o u g h t to b e the first ones to acquire a mature, i.e.
d i s c h a r g a b l e , condition. Those cnidocytes that occasionally m i g r a t e into the h y p o s t o m a l
e c t o d e r m (Fig. 15; hc) or that are distributed in the h y d r a n t h wall h a v e n e v e r b e e n
o b s e r v e d to b r i n g their capsules to an e r e c t e d position.
Figure 15 shows a d e v e l o p i n g polyp in w h i c h the m o u t h o p e n i n g is just a b o u t to be
formed. The e c t o d e r m a l cells are w i t h d r a w n from the top of the b u l b - s h a p e d hypostome,
while the e n t o d e r m a l layer still acts as a flattened b r i d g e over the p r o s p e c t i v e o p e n i n g .
T h e question of w h e t h e r or how the m e s o l a m e l l a is locally affected at this s t a g e of
d e v e l o p m e n t could not b e definitely a n s w e r e d .
438
C. S o m m e r
N e a r the d e v e l o p i n g mouth, a n e w cell t y p e differentiates in the e n t o d e r m , the
h y p o s t o m a l g r a n u l a cell (Fig. 15; hgc). Its cylindrical to c o n e - s h a p e d b o d y r e s e m b l e s that
of the typical s u p p o r t i n g cells of th e h y p o s t o m a l entoderm, b u t it differs in containing
m a s s e s of m i n u t e acidophilic granules. T h e s e are mainly c o n c e n t r a t e d in t h e apical half
to two-thirds of the cell body.
A n o t h e r sort of g r a n u l a cell, the digestive g l a n d cell, has a l r e a d y b e e n r e c o g n i z e d in
the p l a n u l a e n t o d e r m (see section on "Free planulae"). This cell t y p e is c o n s i d e r a b l y
l a r g e r t h a n the h y p o s t o m a l one. Moreover, it is p r e s e n t d u r i n g the w h o l e of m e t a m o r phosis, a l t h o u g h it d o e s not e x c e e d a m e a n n u m b e r of a b o u t 8-10 p e r a n i m a l until s t a g e 7
(Fig. 17). B e g i n n i n g with s t a g e 7 the f r e q u e n c y of digestive g l a n d ceils i n t h e e n t o d e r m
increases, r e a c h i n g 14-21 p e r a n i m a l at s t a g e 8. Most of t h e m are s i t u a t e d in the
e n t o d e r m of the b a s a l disk a n d the stem, b u t a few h a v e also b e e n i d e n t i f i e d in the
stomach (Fig. 15; dgc). This is r e m a r k a b l e b e c a u s e in full-grown p r i m a r y p o l y p s (see
below), as well as in asexually born stock h y d r a n t h s (Mergner, 1957), no d i g e s t i v e g l a n d
cells are found in the stomach.
S t a g e 9 : M e t a m o r p h o s i s is c o m p l e t e d b y a continuation of the d e v e l o p m e n t a l
trends that started in the p r e c e d i n g stages. The tentacles g r o w to their final l e n g t h of
a b o u t t h r e e or four times that of s t a g e 8, while the formation of n e w b u d s ceases. The full
n u m b e r of tentacles in p r i m a r y p o l y p s varies from 13 to 19 (Fig. 18). E v e n b e f o r e the
tentacles r e a c h t h e i r final length, the mouth b r e a k s o p e n at the oral p o l e of the
hypostome, a p p a r e n t l y by rupture of the e n t o d e r m a l b r i d g e d e s c r i b e d in s t a g e 8. In
u n d i s t u r b e d living polyps, the lips are n o r m a l l y closed tight; b u t w h e n the p o l y p is
excited b y food, or is i n f l u e n c e d b y fixative solution, the h y p o s t o m e o p e n s w i d e a n d
a s s u m e s the s h a p e of a calyx.
The t e n t a c u l a r e c t o d e r m consists of flattened e p i t h e l i o m u s c u l a r cells a n d i r r e g u l a r l y
distributed cnidocytes, most of w h i c h h a v e e r e c t e d their capsules in a position r e a d y for
firing (Fig. 16; e r c n ) . All cnidocytes can b e identified as microbasic e u r y t e l e s b y the
p r e s e n c e of a typical acidophilic stylet lying slightly oblique to the l o n g i t u d i n a l axis of the
capsule. At h i g h magnifications, t h e small, l e n s - s h a p e d nucleus of a c n i d o c y t e can b e
s e e n lying n e a r to or in close contact with the capsule at its b l u n t end.
The differentiation of the g l a n d cell ring (Fig. 16; gcr) s u r r o u n d i n g the b a s e of the
h y d r a n t h is a d v a n c e d , as d e m o n s t r a t e d b y a further i n c r e a s e of t h e c y t o p l a s m a t i c
stainability with basic dyes. The ring has an oral-aboral m e a s u r e m e n t of o n l y o n e or two
cell dimensions. Orally, it is s e p a r a t e d from the n e i g h b o u r i n g e c t o d e r m a l cells b y a ringfurrow that d e e p l y intersects the e p i t h e l i u m so that the m e s o l a m e l l a is g e n e r a l l y laid free
over a small d i s t a n c e (Fig. 16; rf).
A v e r y delicate film of p e r i d e r m covers the g l a n d cell r i n g a n d c o n t i n u e s a b o r a l l y
over the b a s e of the hydranth, the constricted "neck" r e g i o n (Fig. 16; nc), t h e stem, a n d
the foot. H e r e it b e c o m e s g r a d u a l l y thicker, with a single a b r u p t i n c r e a s e in thickness
b e t w e e n n e c k to stem. In living p r i m a r y polyps, the stem w a s o b s e r v e d to g r o w r a t h e r
quickly. C o n s i d e r i n g its morphology, it can b e d e r i v e d that p e r i d e r m is p r i m a r i l y f o r m e d
b y the cells of the g l a n d ring, t h e n m o v e d aborally, while n e w m a t e r i a l is s e c r e t e d from
the following e c t o d e r m a l cells a n d a t t a c h e d to the i n n e r surface of the tube. In s u p p o r t of
this, acidophilic g r a n u l e s that m i g h t r e p r e s e n t precursory secretion m a t e r i a l are often
found n e a r the a p i c e s of the e c t o d e r m a l cells of t h e h y d r a n t h base, the neck, a n d the
u p p e r stem (Fig. 16; g).
Larval d e v e l o p m e n t a n d metamorphosis of E u d e n d r i u m
racemosum
m
a
er Cn
t
nC
/.:i~
l • ./.':'I'
Fig. 16, E u d e n d r i u m r a c e m o s u m , Stage 9. Fully developed primary polyp. Scale: 100 ~m
439
C. S o m m e r
440
~32"
2O
~28"
18
16
9~ 2o
U
c,
"~ lO4~12"
~ 4
o
8'
z
4.
(8)
)
(6)
2"
17
J
i
,
0
1
2
|
3
4
Stage
5
~
1
,
i
6
7
8
9
ii
o
18
&
z2
i'6
2o
Time after hatching (h)
Figs 17-18. Eudendrium racemosum. 17. Increase in number of digestive gland ceils during
metamorphosis. Bars show standard deviations. 18. Successive numbers of tentacles during stages 6
to 9. Numbers in brackets give the respective stages. Bars show standard deviations
Differentiation of the e n t o d e r m has p r o c e e d e d in a m a n n e r that e n a b l e s t h e o r g a n i s m
to c h a n g e from lecithotrophic to planktotrophic nutrition. The h y p o s t o m a l g r a n u l a cells
n
(Fig. 16; hgc) h a v e i n c r e a s e d in n u m b e r a n d are more w i d e l y d i s t r i b u t e d over the
h y p o s t o m a l e n t o d e r m t h a n in s t a g e 8. The intraceUular storage of the g r a n u l e s t o w a r d s
the cell a p e x p r o b a b l y indicates their secretory nature. T h e function of the s e c r e t e d
s u b s t a n c e m a y b e digestive (cf. Bouillon, 1966, in Halocordfle disticha) or a d h e s i v e
(ensuring the i n t a k e of food o r g a n i s m s c a u g h t b y the tentacles), or both.
The g a s t r o d e r m a l cells of the stomach a n d n e c k are almost uniform in s h a p e b u t
d e c r e a s e in size t o w a r d s the latter. Yolk particles are scarce in the s t o m a c h cells a n d
a b s e n t in the n e c k region. Digestive g l a n d cells are a b s e n t from b o t h regions. At t h e
tentacle b a s e s the g a s t r o d e r m builds a f u n n e l - s h a p e d , b h n d - e n d i n g d u c t t h a t is followed
b y a row of l a r g e t e n t a c u l a r axial cells (Fig. 16; tac). Each possesses a c e n t r a l l y l y i n g
nucleus a n d a h i g h l y v a c u o l a t e d cytoplasm.
The e n t o d e r m of the stem a n d foot differs from that of the stomach a n d n e c k in two
respects: (1) digestive g l a n d cells are p r e s e n t in high n u m b e r s ; their a b u n d a n c e has e v e n
i n c r e a s e d since s t a g e 8 (see Fig. 17); (2) the e n t o d e r m a l cells lining the g a s t r a l cavity of
stem a n d foot h a v e b y n o w d e v e l o p e d intracellular vesicles. T h e s e stain w e a k l y with
acidic dyes a n d are distributed without any preferential location in the cytoplasm.
W h e t h e r t h e y r e p r e s e n t a particular t y p e of secretory vesicles or m i g h t b e i n v o l v e d in the
intracellular d i g e s t i o n of p h a g o c y t o z e d food particles cannot b e d e c i d e d at present.
Larval development and metamorphosis of Eudendrium racemosum
441
DISCUSSION
The general body organization of the planula of Eudendrium racemosum and its
metamorphosis into the p~,nary polyp is consistent with the majority of facts known from
several species from other hydroid famihes. For example, the initial differentiation of icells, cnidoblasts, and premature cnidocytes in the larval entoderm has been confirmed to
be common to all hydroid species that pass through a planula stage in their development
(Harm, 1903; Mergner, 1957, 1971; Wefler-Stolt, 1960; B4nard-Boirard, 1962; Cowden,
1965; van de Vyver, 1964, 1967; Bodo & Bouillon, 1968; Summers & Haynes, 1969; Martin
& Thomas, 1977; Martin et al., 1983; Martin & Archer, 1986a). In several species, a few
premature cnidocytes penetrate the mesolamella as early as the planula stage and are
erected in the ectoderm, for example in Hydractinia echinata (see van de Vyver, 1964),
Cordylophora caspia (see van de Vyver, 1967), and Phiafidium h e m i s p h a e r i c u m (see
Bodo & Bouillon, 1968). These are said either to have a defensive function or to play a role
in the larva's attachment to the substratum, the latter being demonstrated in Hydractinia
echinata alone (Chia & Bickell, 1978). Premature cnidocytes were occasionally found in
the ectoderm of planulae of Eudendrium racemosum too, but always in very low numbers
and never erected in a position for discharge. In all of the investigated species, a mass
emigration of i-cells, cnidoblasts, and premature cnidocytes occurs in connection with
metamorphosis.
A mucus-secreting cell type occurs in the ectodermal layer of K r a c e m o s u m a n d in
all other hydroid planulae so far examined. Secretion certainly facilitates settlement at
the end of the larval period, due to the stickiness of the hberated mucus (Wasserthal &
Wasserthal, 1973).
A second type of secretory cell has been demonstrated in the larval ectoderm of a few
species, namely Phiah'dium hemisphaericum, Obelia sp.,' Sarsia eximia (see Bodo &
Bouillon, 1968), and Coryne muscoides (see van de Vyver, 1967). It was n a m e d "cellule
glandulaire sph4ruleuse ectodermique". Cells with similar morphology, distribution, and.
acidophilic granules, were described as "kleine sekretorische Zellen" (small secretory
cells) in Eudendrium armature (see Wasserthal & Wasserthai, 1973), and a p p e a r to be
homologous with those found here in K racemosum. It should be emphasized, however,
that another group of granula-containing cells has been discovered in the planula of E.
racemosum, the so-called sensory-nervous cells (Mergner, 1957). They are morphologically different from the above-mentioned secretory cells in possessing one or more long,
sometimes ramified plasma processes running from the cell body into the lateral or apical
interstitium. In view of the similarity between the two cell types in question it cannot be
definitely decided whether they are truly distinct or not. In the latter case, all of them
might be representatives of a neurosecretory cell that occurs in diverse morphological
forms over the ectoderm. In fact, sensory as well as nervous cells with conspicuous
neurosecretory granules have frequently been recognized in recent electron microscopic
investigations of hydroid planulae (Martin & Thomas, 1980, 1981b; Martin et al., 1983;
Weis et ai., 1985; Thomas et al., 1987).
Contrasting opinions are d e b a t e d in the literature concerning the fate of ectodermal
mucous cells during metamorphosis. In many species, the mucous cells are reported to be
completely emptied within a few minutes after attachment (Bonner, 1955; van de Vyver,
1964, 1967, 1968a, b; van de Vyver & Bouillon, 1969; Bodo & Bouillon, 1968; Korn, 1966).
442
C. S o m m e r
V a n de Vyver (1964) r e p o r t e d that in the p l a n u l a e of Hydractinia echinata the r u d i m e n t s
of m u c o u s cell b o d i e s then d e g e n e r a t e in the ectoderm. E x a m i n i n g s e t t l e m e n t a n d
m e t a m o r p h o s i s in the same s p e c i e s . b y use of electron microscopy, W e i s & Buss (1987)
also found that mucous cells display an i n c r e a s e d secretory activity d u r i n g a t t a c h m e n t
b u t t h e n d i s a p p e a r from the e c t o d e r m b y m o v i n g across the m e s o l a m e l l a into the
e n t o d e r m . H e r e they u n d e r g o lysis, a n d n u m e r o u s large mucous vesicles c a n b e o b s e r v e d
floating in the gastral cavity. The results o b t a i n e d in the p r e s e n t s t u d y o n E. r a c e m o s u m
clearly c o r r e s p o n d with the l a s t - m e n t i o n e d view. B e g i n n i n g at s t a g e 2, first the m u c o u s
cells of the b a s a l a d h e s i v e region p e n e t r a t e the m e s o l a m e l l a a n d i m m i g r a t e into the
e n t o d e r m , followed b y those of the u p p e r ectoderm. This m o v e m e n t c o m e s to an e n d
d u r i n g stage 3. Subsequently, i n c r e a s i n g a m o u n t s of mucus can b e d e t e c t e d histochemically within the gastral lumen. Hence, it s e e m s highly p r o b a b l e that v a l u a b l e organic
m a t t e r is "recycled" b y w a y of digestion. Pnture investigations m u s t s h o w w h e t h e r E.
r a c e m o s u m a n d H. echinata are e x c e p t i o n a l in this r e s p e c t or if the p r o c e s s of m u c o u s cell
i m m i g r a t i o n has so far b e e n o v e r l o o k e d in other species.
S u b s e q u e n t to the immigration of m u c o u s cells, m a s s e s of i-cells, cnidoblasts, a n d
p r e m a t u r e cnidocytes migrate from the e n t o d e r m to the ectoderm. T h e role of e c t o d e r m a l
i-cells in m e t a m o r p h o s i s is not clear. Beside their differentiation into cnidoblasts, WeilerStolt (1960) c o n c l u d e d from hght microscopic observations on Eleutheria dichotoma that
n u m e r o u s i-cells p a r t i c i p a t e d in the formation of the h y p o s t o m e a n d the tentacles. This
finding is not confirmed by the p r e s e n t results from E. racemosum. Prom s t a g e 3 onwards,
i-cells are a b u n d a n t only in the e c t o d e r m of the u p p e r b a s a l disk a n d of t h e d e v e l o p i n g
stem, a n d are rarely p r e s e n t in the h y d r a n t h wall. N o n e could b e f o u n d in the t e n t a c u l a r
a n d h y p o s t o m a l regions. Hence, in E. racemosum, cells differentiating in t h e e c t o d e r m or
e n t o d e r m of the tentacles a n d the h y p o s t o m e are b e l i e v e d to d e r i v e from normal
e p i t h e h a l cells. E x a m p l e s are the t e n t a c u l a r axial cells a n d the h y p o s t o m a l g r a n u l a cells,
The s e q u e n c e of tentacle b u d d i n g d u r i n g late m e t a m o r p h o s i s is p o o r l y known.
Primary polyps with i r r e g u l a r l y - d i s p e r s e d tentacles, or with tentacles a r r a n g e d in several
whorls, d e v e l o p the more oral tentacles first, t h e n a n e q u a l n u m b e r b e l o w the first whorl
a n d so on. A typical s e q u e n c e is 4, 8, 12 etc. Such a s e q u e n c e has b e e n d e s c r i b e d in Clava
multicornis b y H a r m (1903) a n d Turritopsis nutricula b y Brooks & R i t t e n h o u s e (1906).
A t h e c a t e h y d r a n t h s with only one whorl form a p r i m a r y set of t e n t a c l e s t h a t is d o u b l e d
after a time. P o r example, the s e q u e n c e 5, 10 w a s d e s c r i b e d in Stomotoca apicata (=
A m p h i n e m a dinema) b y Rittenhouse (1910) a n d 10, 20 in E u d e n d r i u m r a m o s u m b y
A l l m a n (1871). In contrast, the observations focused on this point in E. r a c e m o s u m l e d to
a n o t h e r result. D e v e l o p m e n t starts with the b u d d i n g of 6 or 7 tentacle a n l a g e s at s t a g e 6,
followed irregularly b y the formation of n e w b u d s b e t w e e n the b a s e s of t h e o u t g r o w i n g
o l d e r tentacles. This p r o c e e d s g r a d u a l l y more slowly until s t a g e 9, w h e n a n u m b e r of
13-19 is reached. A l t h o u g h the n u m b e r is h i g h e r in h y d r a n t h s of a n a d u l t colony (about
28-35 after Wengler, 1974}, the p r i m a r y polyp does not b u d further tentacles. Consequently, it must b e s u g g e s t e d that tentacle formation a g a i n starts w h e n the postm e t a m o r p h i c p o l y p c h a n g e s into a c o m p l e x a n i m a l colony b y a s e x u a l r e p r o d u c t i o n .
N e i t h e r is the p r i m a r y polyp a true "adult" with r e g a r d to its cnidome. It h a s b e e n
p o i n t e d out that all c n i d a e on the tentacles - or, in a p r e m a t u r e state, in t h e e c t o d e r m of
foot a n d stem - are exclusively microbasic euryteles. Likewise, this fact w a s also stated in
the planula. H o w e v e r , a second t y p e of cnidocyst occurs in colonial h y d r a n t h s , n a m e l y
a
L a r v a l d e v e l o p m e n t a n d m e t a m o r p h o s i s of E u d e n d n u m
racemosum
443
t h e a t r i c h o u s i s o r h i z a (cf. M e r g n e r , 1957, as " G l u t i n a n t e n " ; a n d W a t s o n , 1985). P r o b a b l y
this s e c o n d t y p e p e r f o r m s f u n c t i o n s for w h i c h t h e r e is n o r e q u i r e m e n t i n t h e p r i m a r y
polyp.
A c k n o w l e d g e m e n t s . I wish to express my sincere thanks to Prof. Dr. H. M e r g n e r for supervising the
investigation and for his constructive criticism on the manuscript. I am i n d e b t e d also to Dr. G.
Bavestrello for his valuable help during my guest-stay at the Zoological Institute of the University of
Genoa, Italy. For linguistic comments on the text, I t h a n k Dr. P. F. S. Cornelius from the British
M u s e u m (Natural History), London.
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