Old and new data on Seisonidea (Rotifera)

Abstract

Class Seisonidea consists of one marine genus, Seison, with two species (S. nebaliae and S. annulatus) which are epizoic on the crustacean Nebalia. Seisonidea are the only rotifers whose reproduction is strictly bisexual. They also possess the unusual feature of having well-developed males. In this paper we review the literature concerning biogeographical distribution, relationships with their host, and morphology, and present new information obtained with SEM and optical microscopy of both living animals and serial sections.
Some seisonid characters, such as the paired retrocerebral organ, nervous system, and trophi, suggest that they hold a primitive position within phylum Rotifera. However, they do share features with other rotifers: paired gonads and an unusual locomotory behavior with Bdelloidea; lateral antennae, cellular stomach wall, arrangement of intracytoplasmic lamina, and other characters with Monogononta. Some features are peculiar to Seison: obligatory amphimixis, endolecythal eggs, encysted spermatozoa, unique mastax, and absence of copulatory organ in males and of vitellaria in females. Reduction of the corona and absence of resistant stages in Seisonidea may be related to their habitat and to their life style. We propose a closer relationship of Seisonidea to Monogononta than previously asserted.

Full text

Hydrobiologia 255/256 : 495-511, 1993
.
J
. J
. Gilbert, E
. Lubzens & M
. R
. Miracle (eds), Rotifer Symposium VI
.
© 1993 Kluwer Academic Publishers
. Printed in Belgium
.
Old and new data on Seisonidea (Rotifera)
Claudia Ricci
1
,
Giulio Melone
2
& Cnstma Sotgia
'Department of Animal Biology, University of Torino, Via Accademia Albertina 17, 10123 Torino, Italy
;
2
Department of Biology, University of Milan, Via Celoria 26, 20133 Milano, Italy
Key
words
:
Biology, geographical distribution, morphology, phylogeny, Rotifera,
Seison,
Seisonidea
Abstract
Class Seisonidea consists of one marine genus,
Seison,
with two species
(S
.
nebaliae
and
S
.
annulatus)
which are epizoic on the crustacean
Nebalia
.
Seisonidea are the only rotifers whose reproduction is
strictly bisexual
. They also possess the unusual feature of having well-developed males
. In this paper
we review the literature concerning biogeographical distribution, relationships with their host, and mor-
phology, and present new information obtained with SEM and optical microscopy of both living ani-
mals and serial sections
.
Some seisonid characters, such as the paired retrocerebral organ, nervous system, and trophi, sug-
gest that they hold a primitive position within phylum Rotifera
. However, they do share features with
other rotifers
: paired gonads and an unusual locomotory behavior with Bdelloidea
; lateral antennae,
cellular stomach wall, arrangement of intracytoplasmic lamina, and other characters with Monogononta
.
Some features are peculiar to
Seison
:
obligatory amphimixis, endolecythal eggs, encysted spermatozoa,
unique mastax, and absence of copulatory organ in males and of vitellaria in females
. Reduction of the
corona and absence of resistant stages in Seisonidea may be related to their habitat and to their life style
.
We propose a closer relationship of Seisonidea to Monogononta than previously asserted
.
Introduction
The monogenic Seisonidea is a unique class of
marine rotifers comprising only two species
. Un-
like the rest of the phylum, these rotifers repro-
duce bisexually and possess fully-developed
males which co-occur with females at all times of
the year . They also are the only rotifers which
have no resistant forms
. Because parthenogene-
sis probably evolved from bisexual reproduction
(the opposite is unlikely), Seisonidea may be as-
sumed to be a remnant of ancestral rotifers that
inhabited the bottom of the sea
. Some research-
ers, recognizing the unusual features of seisonids
have concluded that they are a very primitive
group of rotifers (e
.g
.,
Remane, 1929-33
; Epp &
Lewis, 1979
; Wallace & Colburn, 1989)
. Because
of the probable closeness of seisonids to ances-
tral rotifers, study of their biology and morphol-
ogy should help elucidate the evolutionary path-
ways followed by phylum Rotifera
. Here we
review the biology of Seisonidea and attempt to
assess their evolutionary relationship to the other
Rotifera
.
Taxonomy
Class Seisonidea consists of a single order,
Seisonida, comprising a unique family, Seiso-
495

4 96
nidae, with only one genus,
Seison
. Two
species
are recognizable, nevertheless several authors
who described Seisonidea during the last century
confused the taxonomy by giving different names
to the same species
. According to revisions made
by Illgen (1916) and Remane (1929-33), the two
species are
(1) Seison nebaliae
Grube, 1861
(= Saccobdella nebaliae
van Beneden & Hesse,
1864 = Seison grubei
Claus, 1876) and
(2)
Seison
annulatus
Claus, 1876
(= Paraseison asplanchnus
Plate, 1887)
. Other species were described by
Plate (1887),
Paraseison nudus, Ps
proboscideus
and
P
. ciliatus,
but they must be considered
nom-
ina nuda,
being insufficiently described and never
again reported
.
Biology
Both
Seison
species live epizoic only on the lep-
tostracan crustacean
Nebalia
(Plate
I-a)
.
Illgen
(1916) found a single
Nebalia
carrying as many as
100 animals (species not specified) without any
difficulty
. We observed up to
12
S
. nebaliae
on a
single
N
. bipes,
which was able to swim without
impediment
. Biogeographically
Seison
have been
found on
Nebalia
in samples collected from the
coastal bottom at Trieste (Grube, 1861
; Claus,
1876
; Illgen, 1916), Naples (Plate, 1887, 1888
;
Illgen, 1916), Marseille (Marion, 1872) and the
Venice lagoon (pers
. obs
.), in the Mediterranean
Sea
; at Roscoff (de Beauchamp, 1909
; Remane,
1929-33
; Koste, 1975) in the English Channel
; at
Morro Bay, California (Menzies & Mohr, 1952)
in the Pacific Ocean
; at McMurdo Sound and
Magellanic Chile (Leung & Mohr, 1969) in the
Antarctic Sea
.
Of
course, distribution
of Seison
overlaps with that of Nebalia,
but these leptost-
racans are rather poorly known
. Their distribu-
tion appears to be very wide, with a single species,
Nebalia bipes
(Fabricius), in the coastal waters
of
Europe and, possibly,
of North America
.
Plate
I
.
SEM micrographs of
Seison nebaliae
.
Fig
. a
.
Lateral view of
Nebalia bipes
with rotifers (arrow)
.
Fig
. b
.
Ventral view of a young male
: H, head ; N, neck
; T, trunk
; F, foot
.
Seison annulatus
and
S
. nebaliae
often are re-
ported to occur together on the same host, how-
ever the former lives on pleopods while the latter
attaches to pereiopods, edges of
the carapace,
and occasionally to the antennae and abdomen
(Claus,
1876
; Illgen,
1916
; d'Hondt,
1970)
(Plate
I-c)
.
Both species appear to live on
Nebalia
exclusively
; other crustaceans in the same sample
with
Nebalia
never carry
Seison,
but the biologi-
cal relationship between the rotifers and these
leptostracans is uncertain
.
Some authors (Plate, 1887, 1888
; Illgen, 1916
;
Koste, 1975) observed that the stomach contents
of S
. annulatus are the same color as the eggs
of
Nebalia
and argued a possible parasitism of the
rotifer on the crustacean eggs
. In theory, this is
possible, as
N
. bipes
incubates its eggs on the ple-
opods till they hatch into miniature adults
; the
same position is occupied by
S
. annulatus,
which
could easily feed on its hosts' eggs
. However,
because it is thought that the crustacean is unable
to reproduce throughout the year, an alternative
food for the rotifer should be assumed
. The stom-
ach
of S
. nebaliae
contains detritus and algae (Il-
lgen, 1916
; pers
. obs
.), therefore its relationship
with the host may be phoretic or commensal
.
Both
Seison
species are unable to swim and
move only by creeping, but they do not move
easily
. One way rotifers colonize young crusta-
ceans is to move to them when they are still in the
brood chamber (Illgen, 1916
; pers . obs
.)
. How-
ever, it is not known how
Seison
transfer during
the crustacean moult
. Illgen (1916) reported that
isolated
Seison
were able to attach themselves to
a free swimming Nebalia
in an experimental ves-
sel, but we were unsuccessful in repeating this
observation
.
Morphology
Although many studies have dealt with Seisonidea
morphology (Grube, 1861
; Claus, 1876
; Plate,

Fig
.
c
.
A group of rotifers
: e, eggs
.
Fig
.
d
.
Ventral view of the head of two males
: c, corona ; g, ventral groove
.
Fig
.
e
.
Ventral view of the apical pseudosegments bearing rostrum
(ro),
ciliar tufts (t) and mouth
.
4
97

4 9
8
1887
; de Beauchamp, 1909
; Remane, 1929-33
;
Koste, 1975), several issues remain unclear
. Fol-
lowing we review the morphology of seisonids,
adding new information obtained by SEM, TEM,
and optical microscopy
. Unless specified all mor-
phological information refers to
S
.
nebaliae
.
Both species are very similar, apparently dif-
fering in minor characters
. The body of
Seison
can be divided into four parts
: head, neck, trunk,
and foot
. Neck and foot are segmented and can
be retracted telescopically, while head and trunk
are not segmented (Plate I-b)
.
Seison nebaliae is
generally larger than
S
. annulatus
.
Plate (1887,
1888) reports about 1 mm for females of
S
.
an-
nulatus,
which are larger than their males, 0
.4-
0
.7 mm long
. The opposite is true for
S
. nebaliae,
which were reported to reach the length of 2
.5 mm
(Remane, 1929-33)
. Our male specimens of
S
. nebaliae
are about 1
.1 mm long and the fe-
males 0
.8 mm long
.
Head
The head is oval and somewhat flattened laterally
(Plate I-b
; II-a,c)
. In mature specimens, it is about
130-150 µm long and about 50-60,am wide
. Many
secretory cells with granular cytoplasm are
present in the central and posterior regions, close
to the brain
. The mastax, with its strong muscles,
is visible apically
. No eyes are evident
. A sort of
ventral longitudinal groove, shaped like a spoon,
is seen in males, but this feature is almost lack-
ing in females (Plate I-b,d
; Fig
. 1)
.
Neck
Made of three regions, the neck is about 250-
280 tm long
. The first region in
S
. nebaliae
bears
dt
Fig
. 1
. Seison nebaliae
:
scheme of the head with brain, retro-
cerebral apparatus and tasters
. A
: dorsal view
. B
: lateral view
.
b, brain
; rg, retrocerebral gland
; sg, subcerebral gland
; tg,
taster gland
; dt, dorsal taster
; It, lateral taster
; db, dorsal lobe
of the brain
; vb, ventral lobe of the brain
; m, mastax
; mg,
mastax ganglion
(?)
; e, esophagus
.
four rings (Plate I-b
; II-c) and in
S
.
annulatus
two
or three
. The neck can be withdrawn into the
ventral part of the trunk
; it contains ducts of
cephalic glands and of the excretory system,
esophagus, and muscles
.
Trunk
The trunk is generally oval, tapering posteriorly,
raised dorsally (more so in males than in females)
and flattened ventrally, with longitudinal folds
Plate II
.
Head of
S
.
nebaliae
.
Fig
. a
.
Lateral view of living rotifer at light microscope
: ma, mastax
; s, salivary gland
; dt, dorsal taster
(
= antenna)
; rg, retrocerebral
gland
; sg, subcerebral gland
; tg, taster gland
. x 380
.
Fig
. b
.
Mastax at the light microscope
: f, fulcrum
; m, manubrium
; r, ramus
. x 1500
.
Fig
. c
.
SEM dorsal view
: ro, rostrum
; dt, dorsal taster
; It, lateral taster
.
Fig
. d
.
Detail of Fig
. c
: dt, dorsal taster
; It, lateral taster
.

4
9
9
Fig
. e,
f,
g
.
Histological sections
.
Fig
. e
.
Cross section of rear head
: tg, taster gland
; sg, subcerebral gland
. x 450
.
Fig
.
f
Parasagittal section
: ro, rostrum
; dt, dorsal taster
; rg, retrocerebral gland
; tg, taster gland
; b, brain
; sg, subcerebral gland
.
Continuous line refers to the section in Fig . e and broken line to Fig
. g
. x 450
.
Fig
. g
.
Dorsal taster (dt) and brain (b),
connections toward lateral antennae (arrows)
. x 720
.

5
00
Plate III
.
Fig
. a, b
.
Epidermal syncytium (s) with intracytoplasmic lamina
(1),
and muscles (m)
.
Fig
. a x 4000
; Fig
. b x 20000
.
Fig
. c
.
Foot with adhesive disc at SEM
: t, tubercule with the opening of mucous gland cell, and its secretion
.
Fig
.
d
.
Lateral view of the foot with cement glands (fg) of living rotifer at light microscope
. x 320
.
Fig
. e
.
TEM image of cross section of the neck
: e, esophagus lined with cuticle and surrounded by muscular sheath
(ms)
; ex,
excretory duct
. x 16000
.
Fig
.
f
.
TEM image of cross section of the anterior part of the trunk
: ex, excretory duct
; fc, flame cell
. x 11200
.

(Plate I-b, c)
. The same is true for S
. annulatus,
except for the hump, which is almost lacking,
giving its trunk a more slender appearance
. Seison
annulatus also exhibits four discernable constric-
tions on the rear trunk, which gives it the name
.
The trunk of S
. nebaliae is slightly compressed
laterally and about 230-290 µm long
. It contains
the stomach sac, the very small intestine, and a
voluminous genital apparatus (Plate IV)
.
Foot
The foot (ca 250-280 µm long) is segmented into
four parts in S
. nebaliae (Plate I-b
; III-d) and
possibly into six parts in S
. annulatus (Claus,
1876
; Plate, 1887, 1888
; de Beauchamp, 1909
;
Koste, 1975)
. It contains many ducts and adhe-
sive glands of different lengths
. Some glands open
at different positions along the foot and look like
cutaneous glands
. Most open at the terminal ad-
hesive disc, which is surrounded by a cuticular
ring
. The last segment of the foot, ending with the
disc, is always bent dorsally
. Ventrally it pos-
sesses a tubercle, which is the opening of a mu-
cous gland (Plate III-c)
.
Integument
As in other rotifers (e
.g
., Clement, 1980) the body
is covered with a more or less continuous syncy-
tial integument with a dense intracytoplasmic
lamina perforated by pores connected to bulbs
(Plate III-a,b)
. The lamina is thick (about 1
.0 µm)
and rigid, but it thins to about 0 .6 µm at articu-
lating regions
. Generally, the lamina is uniformly
made up of stacked lamellae resembling the 'No-
tommata type' described by Clement (1980)
. A
few images of the trunk reveal a thickened basal
layer in addition to the lamellae
.
Corona
The external morphology of the head reveals two
apical pseudosegments that can be retracted tele-
scopically
. The first one forms a mobile lobe, the
rostrum, which can cover the ventral mouth
(Plate I-e
; II-f)
. The mouth opens within a ciliated
buccal field lined bilaterally by five or six mobile
ciliar tufts arranged in a row
. Ventrally, the mouth
is bordered by a V-shaped, bilobed structure with
short cilia on its inner edge
.
Remane (1929-3 3) considers the Seison corona
to be secondarily reduced, similar to the 'As-
planchna type' of de Beauchamp (1909), with the
apical field strongly decreased
; the ciliary tufts are
considered to be a reduced paracingulum
. But, in
our opinion, the arrangement of the coronal cilia
recalls the `Euchlanis type' described by de Beau-
champ (1909) (Fig
. 2)
. If true, the lateral ciliary
tufts may be considered homologous to the tro-
chus and the ventral cilia to the cingulum, thereby
delimiting a finely ciliated buccal field
. Plate (1887,
1888) observed two pairs of ciliary tufts in S
. an-
nulatus, which he called tactile setae, assuming
them to be sensory structures
. However, it must
be pointed out that the entire structure cannot be
resolved in detail in S
. nebaliae and, perhaps in
S
. annulatus as well, by optical microscopy
.
The thin disposition of cilia and the small ex-
tension of the entire rotatory organ compared to
the size of the head (1
:10 in length) (Plate I-d) and
of the body, suggests a poor performance in gath-
ering and conveying particulate food to the mouth
.
However, the 'trochus' cilia move from the exte-
rior toward the mouth opening, suggesting an ac-
tive function in collecting or pushing food into the
mouth, aided by the peristaltic movements of the
proximal digestive system
. A sensory function of
the rotatory organ cannot be excluded
.
5
0
1
Fig
. 2
. Schematic rotatory apparatus of Seison nebaliae
. Large
dots represent lateral tufts
.

5
02
Plate IV
.
Fig
. a, b, c, d, e,
f
.
Sequence of cross sections through anterior part of the trunk of adult male
. n, retracted neck
; gg, gastric glands
;
e, esophagus
; vd, vas deferens
; t, testis
; st, stomach ; ex, excretory apparatus
; c, cytophore
; es, encysted spermatozoa
; cb, cili-
ated bulb
; arrow, beginning of the intestine
. x 470

Digestive tract
As previously reported, the digestive system is
composed of pharynx with mastax, long esopha-
gus, oval stomach, and short intestine with anus
(Remane, 1929-33)
. Many glands open at differ-
ent levels along the digestive system
.
Although originally described as virgate (de
Beauchamp, 1909), the mastax is known to be
fulcrate (Remane, 1929-33)
. The trophi consists
of paired manubria, rami and unci, and an elon-
gated fulcrum (Plate II-a, b) (see also Koste,
1975)
. All pieces look to be loosely arranged and
connected to a cuticular sheath
. Generally, the
mastax shape is similar in both species
. However,
the fulcrum is smaller in
S
. nebaliae,
while the
manubria are elongated in
S
. nebaliae
and leaf-
like in
S
.
annulatus
(Remane, 1929-33)
. The mas-
tax occupies an anterior position, so that the
proximal part of the fulcrum can protrude from
the mouth
. Movement of both esophagus and
pharynx, as observed in living specimens, is peri-
staltic and pump-like
. This has suggested to many
authors that the mastax can perforate host eggs
and suck out the contents
(e
.g
.
Koste, 1975)
.
The pharynx is reached by ducts from a pair of
elongate, unicellular salivary glands, located ven-
trally and extending along most of the length of
the head (Claus, 1876
; Plate, 1887, 1888)
(Plate II-a)
. Smaller unicellular glands reach the
anterior part of the slender esophagus
(ca
7,4m in
diameter)
. It is lined with cuticle and surrounded
by a muscular sheath (Plate III-e)
. The esophagus
extends along the neck to the stomach in the
trunk
. At the posterior end of the head, a few
flask-shaped glands [five in
S
. nebaliae,
two in
S
. annulatus
(Plate, 1887, 1888)] possess ducts
which run along the esophagus
. Plate (1887, 1888)
considered them to be esophageal glands, but
Claus (1876) and Remane (1929-33) believed
them to be cutaneous glands
. Some ducts appear
to open on the dorsal neck, and therefore, at least
some of them are cutaneous glands
. Where the
esophagus reaches the stomach, four gastric
glands are present (Plate IV-a), but previous au-
thors have described different number of glands
in this region
:
[ca 10
in
S
. nebaliae
(Remane,
5
0
3
1929-33)
; 2 in
S
. annulatus
(de Beauchamp,
1909)
; numerous in S
.
annulatus
(Koste, 1975)]
.
The esophagus joins the stomach with a large
protrusion
.
The stomach wall is made of large polygonal,
uninucleate cells lacking cilia, which are arranged
in six longitudinal rows (Plate IVb-e)
. Its appear-
ance can vary, probably according to the nutri-
tional status of the animal
. The stomach of
S
. nebaliae
appears as a sac
; in females it occu-
pies a large part, about 2/3 of the trunk, but in
males it is smaller, often hardly visible in living
animals
. The stomach wall contains granules
which may have a secretory function, while the
lumen is covered with microvilli
. The stomach is
followed by a very short and slender intestine,
which is not easily detectable (Fig
. 3)
. Thus, it
appears that the seisonid stomach performs both
digestion and assimilation
.
In females, the intestine is placed posteriorly
and reaches the cloaca dorsally at the end of the
trunk (Fig
. 3B)
. The cloaca opening appears as a
transverse furrow at the connection between the
trunk and the first foot segment
. It is covered by
a fold of cuticle from the foot (Plate V-c, d)
. In
males, the intestine joins the stomach at the mid-
dorsal wall and runs anteriorly reaching the clo-
aca between the neck and trunk (Fig
. 3A)
. It
opens as a transverse furrow covered by a fold of
the trunk integument (Plate
V-a)
.
The intestine of
the male can be seen only with difficulty, because
it is very thin and hidden by the complex genital
apparatus
. In fact, Plate (1887, 1888) claimed that
S
. annulatus
has no intestine and anus, but other
authors were able to recognize the intestine in
both species (Remane, 1929-33)
.
Nervous system
The brain occupies the posterior half of the head
(Fig
. 1)
. It has an outer cellular layer and a uni-
form inner mass of nerve fibers (Plate II-e-g)
.
Around this unpaired structure, and connected to
it, five masses of nervous tissue are visible
. Dorsal
and posterior to the brain one small mass is clearly
connected to an unpaired, short antenna (NB
:
Remane, 1929-33 reports two ganglia)
. One pair

5
0 4
Fig
. 3
. Seison nebaliae
; scheme of the digestive tract and re-
productive apparatus of a male (A) and a female
(B)
.
s,
stomach
; t, testis
; ov, ovary
; sv, seminal vesicle
; vd, was defe-
rens
; cl, cloaca
.
of nerve masses is present in a posterior position
;
they surround the esophagus and possibly give
rise to the principle ventral nerve described by
Remane (1929-3 3)
. Two other nervous structures
are directed anteriorly and ventrally
. They encir-
cle the esophagus and may represent the mastax
ganglia hypothesized by Remane (1929-33)
.
A very small unpaired antenna, the dorsal
taster, lies in a dorsal depression of the head of
S
. nebaliae
.
It consists of an annular thickening
surrounding a small pore measuring about 2
.5 ,am
in diameter
. In the center of the pore a few very
short cilia are found (Plate II-c, d) . In addition to
the nerve mass, the antenna is connected with
two flask-shaped cells which extend posteriorly
(Plate II-e, f)
. They look like secretory cells, but
were assumed to be muscle cells by Remane
(1929-33)
.
Lateral and posterior to the dorsal taster are
located two very small structures which were
barely seen by Illgen (1916)
. Visible by SEM,
these small pores measure about 1 pm in diame-
ter and possibly house three very short cilia
. These
pores connect to the brain (Plate II-c, d) and, in
general, they resemble a small dorsal antenna, but
lack its cuticular ring
. They represent the lateral
antennae, present in many monogononts
. The
dorsal antenna is reported in
S
.
annulatus
(Plate,
1887, 1888
; Koste, 1975), but no mention is made
about the lateral antennae
. No description of the
nervous system of S
.
annulatus is
available
. Other
sensory organs are not visible in either species
.
Retrocerebral glands
In the head, four symmetrically arranged, flask-
shaped cells can be seen
. One pair of these elon-
gate cells is located over the brain, while the sec-
ond larger pair is located ventrally and more
posterio-lateral to the brain (Plate II-e, f)
. Ducts
from all these cells reach the rostrum and open
over the mouth (Fig
. 1)
. There appears to be a
correlation of these cells to similar structures in
other rotifers
. The position of the cells located
over the brain is comparable to that of the un-
paired retrocerebral sac, while the posterio-lateral
cells have the same position as the subcerebral
glands (Remane, 1929-33)
. Moreover, both de
Beauchamp (1909) and Remane (1929-33) argue
that the unpaired retrocerebral sac (RS) might
have originated by fusion of two symmetrical
structures, thus explaining the double ducts re-
tained in the RS of all rotifers
. We agree with this
view and argue that the two glands over the brain

5
0
5
Plate V
.
Fig
. a, b, c
.
SEM images
.
Fig
. a
.
Male cloaca (cl)
;
N, neck
; T, trunk
.
Fig
. b
.
Same view as Fig
. a in a female
.
Fig
.
c
.
Female cloaca (cl)
;
T, trunk
; F, foot
.
Fig
. d, e
.
Light photomicrographs of female genital apparatus
.
Fig
. d
.
Trunk view of living animal
: cl, cloaca
; oc, oocyte with polar body
(pb)
;
st, stomach
; i, intestine
; *, free spermatozoon
.
x 600
.
Fig
. e
.
Parasagittal section of the trunk
: g, germarium
; oc, oocyte
; gg, gastric gland
; st, stomach
; ex, excretory apparatus
. x 450
.
should be considered to be homologous to the
attachment and subsequently its function has
RS
. In addition, both previous authors advanced
changed according to the habitats occupied by
the hypothesis that the retrocerebral apparatus
the different species of rotifers
.
Seison
commonly
could originally secrete a cement for temporary
~
creeps like a leech and the secretion of adhesive

5
0
6
material on its head may be helpful or even nec-
essary for its locomotion
.
Excretory apparatus
A bladder is lacking in
Seison,
but the general
organization of the excretory system is similar to
that of other rotifers
. The excretory apparatus of
S
. nebaliae
(Claus, 1876, 1880
; Illgen, 1914, 1916
;
Remane, 1929-33) and
S
.
annulatus
(Claus, 1876,
1880
; Plate, 1887, 1888 ; Illgen, 1914, 1916 ; Koste,
1975) is as follows
. One paired capillary duct
extendes ventrally from the head to the end of the
trunk
; a paired glandular canal extendes ventrally
along the trunk and joins the capillary duct at the
beginning of the trunk with a flame cell
. The glan-
dular canals join and open in the cloaca of fe-
males, and in the ciliated bulb between seminal
vesicle and vas deferens of males (Illgen, 1914)
.
Seison annulatus
is reported to have 5 pairs of
flame cells : 2 in the head, 1 at the beginning, and
2 at the bottom of the trunk
.
Seison nebaliae
ap-
pears to possess only one pair of flame cells at the
beginning of the trunk
. We were able to locate the
flame cells and glandular canal along the trunk in
both sexes
; the connection to the female cloaca
also was located (Plate III-e, f)
. In addition, in the
ventro-posterior end of the head, is located a
paired glandular structure with thin canalicula
which has the same appearance as the glandular
canal in the trunk
. In the neck, paired capillary
ducts also are visible by TEM
.
Because seisonids dwell in the marine environ-
ment, we assume that osmoregulation is not the
primary role for the protonephridial system, as it
is in freshwaters rotifers (Epp & Lewis, 1979)
.
Instead, the excretory system probably excretes
nitrogen or is related to the maintenance of the
hydrostatic skeleton
.
Seison annulatus
possesses
more flame cells than
S
. nebaliae,
albeit its body
size is smaller
.
Female genital apparatus
The ovary of
Seison
is a sac-like paired structure
containing germarium and growing eggs at differ-
ent stages of maturation
. In mature females it
occupies most of the trunk (Plate V-d, e)
. In the
germarium, small oocytes (evident in some histo-
logical sections) are embedded into a sort of non-
granular matrix which possesses the same stain-
ing properties as cell cytoplasm
. The nuclei of
immature oocytes have large nucleoli and no de-
tectable polar bodies, but growing oocytes always
possess one polar body (Plate
V-d)
.
The eggs do
not appear to possess any envelope
. The small-
est ones have homogeneous cytoplasm and a
rounded nucleus, while the largest ones have
granular cytoplasm and a lobate nucleus . One or
more large nucleoli are present and seem to have
a strong synthetic activity
. The eggs and the ger-
marium inside the two thin-walled sacs are loose
and can move
. The paired ovary sacs unite cau-
dally to form a common oviduct, which opens
into the cloaca
.
The female reproductive system of
Seison
lacks
a vitellarium which is present in both Bdelloidea
and Monogononta (see Gilbert, 198 3 a, 198 8, 198 9
for reviews)
. However, there is a syncytial tissue
surrounding the germ cells (Remane, 1929)
. Nev-
ertheless, seisonid eggs are endolecythal, so the
vitellarium of other rotifers cannot be considered
homologous to this syncytium
. This tissue also is
arranged differently from the follicular layer of
monogononts (Bentfeld, 1971) and bdelloids
(Amsellem & Ricci, 1982)
. Remane (1929-33)
argues that the syncytial tissue of seisonids may
represent a type of seminal receptacle
. Actually,
this is the site at which spermatozoa are concen-
trated in adult females (Remane, 1929-33
; pers
.
obs
.)
. Perhaps it has some function in attracting
spermatozoa to the oocytes after insemination
.
Male genital apparatus
The male genital apparatus is a large U-shaped
structure occupying the major part of the trunk
cavity, partly masking the digestive system (Claus,
1876
; Plate, 1887, 1888
; Illgen, 1914
; Remane,
1929
; Gilbert, 1983b)
. It consists of paired, sac-
like testes, which unite caudally and fold upwards

to form a voluminous, pear-shaped organ, which
lies dorsal to the stomach and reaches the cloa-
cal opening at the beginning of the trunk (Re-
mane, 1929) (Plate IV-a-f)
. Inside the testes,
spermatids at different stages of development are
clustered into loose cytophores
. Caudally, the two
sacs are filled with motile mature spermatozoa,
which enter into the rear of the pear-shaped struc-
ture
. This part may be interpreted as a large sem-
inal vesicle where spermatozoa are oriented and
densely packed (Plate VI-b-d)
. Each sperm is
squeezed into a ciliated bulb, connected to a sec-
ond one, rolled up, and subsequently encysted by
some kind of secretion
. This process has been
estimated to take about 90 seconds (Illgen, 1914)
.
The second enlarged vesicle, constituting the an-
terior part of the pear-shaped body, is completely
filled with encysted spermatozoa and can be con-
sidered a differentiated vas deferens . From this,
a ciliated duct reaches the cloaca (Plate VI-b)
.
Spermatozoa are about 70 µm long (Illgen,
1914), rather uniform in diameter (about 0 .5 µm),
and have a slightly bent, broadly pointed head
(Plate VI-d)
. Encysted spermatozoa are rod-
shaped structures, 8 µm long by 1
.5 µm wide,
rounded at both extremities, and provided at one
end with a sort of flat cap, resembling a saddle
(Plate VI-e)
. The encysted spermatozoon has
been called a spermatophore by all authors
(e
.g
.,
Remane, 1929), but this term commonly refers to
a capsule with many packed spermatozoa inside
.
In seisonids, each spermatozoon is wrapped to
form an immotile structure, thus it seems more
appropriate to call it a encysted spermatozoon
.
Similar structures are commonly found in arach-
nids and other arthropods (see Alberti, 1990)
.
The fine organization of the cyst and spermato-
zoon, and the process of spermatogenesis will be
considered in a separate paper
.
The male genital system of
S
.
annulatus
is sim-
ilar to its congener in its general organization, but
no detailed description is available . Plate (1888)
describes the encysted spermatozoon of
S
.
annu-
latus
as a flask-shaped corpuscle (15 µm long by
5 µm wide) with three divisions
: anterior hemi-
spherical cap, narrower neck, and ovate hind por-
tion
.
Sexual dimorphism
Both sexes are commonly present in a ratio of 1
:1,
but females of
S
.
annulatus
can be more frequent
than males
: i
.e
.,
up to 6
:1 (Plate, 1887, 1888)
.
Apart from the obvious primary sexual charac-
teristics, the two sexes are very similar with noth-
ing
resembling
the strong
reduction
of
monogonont males
.
The overall body shape of
S
.
nebaliae
is slightly
different in the two sexes, with males being gen-
erally larger and slightly humped (Fig
. 3)
. The
opposite seems to hold for
S
.
annulatus
.
In both
species, the digestive system of males is U-shaped,
with the cloaca opening dorsally at the connec-
tion between the neck and trunk
. Exteriorly, the
cloacal opening can be recognized within a deep
fold
. This feature is lacking in females, who have
rectilinear intestines that open into a dorsal clo-
aca at the connection between trunk and foot
(Plate
V-a-c)
.
The genital systems of both sexes open in the
cloaca . In the female, the excretory apparatus
opens into the cloaca
; in the male, it is reported
to open between the seminal vesicle and the vas
deferens (Illgen, 1914)
. We have not been able to
confirm this surprising observation
.
A remarkable character that differs in the two
sexes is the ventral, spoon-shaped groove on the
head (Plate I-d)
.
Present only in males, this struc-
ture may be involved in transfer of spermatozoa
to the female cloaca
. In fact, encysted spermato-
zoa have often been observed attached to the
male head groove (Illgen, 1914, 1916
; pers . obs
.)
.
All other structures
(e
.g
.,
dorsal and lateral an-
tennae, cement glands) are common to both sexes
.
Reproduction
Seisonids reproduce by mixis, with internal fer-
tilization
. Neither Illgen (1914) nor Remane
(1929-33) had the opportunity to observe when
and how it occurs
. The egg seems to be fertilized
when still in the germarium and undergoes the
first meiotic division afterwards (Illgen, 1914)
.
Later, the fertilized egg grows and synthesizes
507

5
0
8
Plate VI
.
Male genital apparatus
.
Fig
. a, b,
c
.
Light photomicrographs of living rotifers
.
Fig
. a
.
Specimen with encysted spermatozoa around the neck (arrow)
.
x 120
.
Fig
. b
.
Cloaca opening (ci) with vas deferens (vd) and seminal vesicle
(sv) connected by ciliated bulb
(cb)
.
x 420
.
Fig
. c
.
Free spermatozoa in seminal vesicle
(sv)
:
cb, ciliated bulb where each spermatozoon is wrapped into the
encysted form
:
vd, vas deferens containing encysted spermatozoa
.
x 1250
.
Fig
.
d
.
Free spermatozoa in the seminal vesicle at SEM
.
Fig
. e
.
Encysted spermatozoa at SEM
.

yolk granules . The second polar body is reported
to be extruded just before the egg is laid
; it de-
velops directly into a miniature adult
.
The egg of
S
. nebaliae is
club-shaped, 155 µm
long by 65 µm wide at its broader tip (Plate
I-c)
.
Although Illgen (1916) describes pedunculate
eggs, we never observed any stalks . The egg of
S
. annulatus is
very similar in shape
. The female
attaches the eggs close to her foot with the pointed
extremity of the egg stuck to the animal's surface,
probably by adhesive secretions from the pedal
glands
. Illgen (1916) argues that the secretion for
the egg adhesion comes from the gland cell that
opens on a tubercle that lies ventrally over the
terminal disc, but this does not seem likely as
both males and females possess this gland
.
Because fertilization is internal and the male
has no copulatory organ, the concern of most
authors
(e
.g
.,
Gilbert, 1989) is how spermatozoa
are transferred
. It must be pointed out that only
free spermatozoa and no encysted sperm have
been observed in the female body
. Contact be-
tween male and female cloaca is possible because
of their positions, but this behavior apparently
has never been observed
. Illgen (1914, 1916) ob-
served males with some encysted sperm attached
to their heads
. On several occasions we were able
to observe males with encysted spermatozoa both
around the first neck segment and attached to the
ventral groove on the head (Plate VI-a)
. Illgen
(1916) speculates that movement of the head may
transfer the sperm to the female cloaca
. Gilbert
(1989) points out that sperm transfer by head
movements does not involve detachment from
the host
. Thus, there is a reduced risk of dislo-
cation which is advantageous to epibiont animals
such as seisonids that move very little
.
Relationships to other rotifers
The overall body shape and locomotion of
seisonids are similar to those of bdelloids, but
there are some striking differences
. The neck is
unique to
Seison,
and while seisonid locomotion
resembles the typical leech-like creeping common
to most bdelloids, the mechanisms differ
. In fact,
5
0
9
bdelloids are able to retract both head and foot
segments telescopically into the trunk while
seisonids cannot
. Seisonids can shorten the neck
and foot telescopically, but are unable to with-
draw the head or to change the trunk shape
. Mus-
cle disposition also is reported to be similar in
seisonids and bdelloids (Remane, 1929-33)
; this
may be related to the creeping locomotion com-
mon to both
. Unfortunately, little is known about
the fine structure of seisonid muscles
. Myofila-
ments of the same size as actin and myosin are
seen, but no obliquely or cross striated fibers have
been detected so far
. Other structures involved in
locomotion, such as well-developed pedal glands
and retrocerebral glands, are common to the two
rotifer classes, but this may represent convergent
evolutionary processes
.
Paired gonads are common to seisonids and
bdelloids, so that they were formerly grouped to-
gether into Digononta (Wesenberg-Lund, 1923)
.
However, Remane (1929-33) argued that this
character is not very meaningful, and many au-
thors (including Remane) stress the absence of
vitellarium in seisonid gonads as being more con-
sequential
. This feature indicates that the egg has
strongly active yolk synthesis in seisonids and is
completely dependent on the vitellarium gland in
other rotifers
.
The major characteristic of seisonids is oblig-
atory amphimixis and, consequently, continual
presence of males
.
Seison
males produce large
amounts of spermatozoa, each one encysted in a
secretion
: a unique feature for rotifers
. Insemina-
tion, too, seems special
. Seisonid males do not
have copulatory organs, while all monogonont
males possess a penis . Further, monogonont
males are not always present with females and
they have various levels of anatomical reduction,
depending on the family
. Males of Seisonidea ex-
hibit fully developed structures, especially their
U-shaped digestive system, with the cloaca in an
anterior position, like that of Flosculariidae males
(Remane, 1929-33)
. Again, as in Flosculariidae
and some Ploima, Seisonidea have no bladders,
but their excretory apparatus is organized the
same way as in other rotifers
: capillary ducts con-
necting flame cells and glandular canals
. Unfor-

5
1
0
tunately, little information is available on seisonid
flame cells, and those are not clear enough to
allow comparisons to the fine organization of
these structures in other rotifers (Clement, 1980)
.
Seison
integument is syncytial and has the in-
tracytoplasmic lamina common to all rotifers
.
Moreover, preliminary observation at TEM
shows it to be arranged in a similar way to the
intracytoplasmic lamina of some monogononts
(i
.e
.,
Notommata),
but it is quite different from that
of bdelloids (Clement, 1980)
.
The specialized way of living of seisonids may
explain the reduction of their corona
. Until we
know exactly what
Seison
feeds on and how, any
attempt to interpret this structure will be specu-
lative
. The stability of the marine habitat of
Seison
may be related to its inability to produce resistant
stages
. Other typical features of seisonids that
may be regarded as more primitive than those of
the other rotifers include mastax, retrocerebral
apparatus, and nervous system
.
The seisonid mastax is special and appears to
be less developed than the trophi of other rotifers
.
It has been hypothesized that the retrocerebral
apparatus has the original function of secreting
adhesive material (Remane, 1929-33)
. Moreover,
the unpaired retrocerebral sacs of bdelloids and
monogononts both retain double ducts and prob-
ably results from merging of two glands
. In
seisonids, the glands are still double, and this can
be considered a primitive condition
. The nervous
system of
Seison consists of a central brain and
a few ganglia ; the anterior ones can be considered
to be the subesophageal mastax ganglion com-
mon to the other rotifers (Remane, 1929-33), but
no ganglia are observed along the body
. How-
ever, their presence cannot be ruled out
. Sensory
structures, such as dorsal and lateral antennae
(tasters) are recognizable and innervated by the
brain
. Bdelloids have no lateral antennae, but they
are common in monogononts, where they can be
found in very different positions
. The dorsal an-
tenna of
Seison is
connected to two glandular
cells
. This might support the hypothesis of Re-
mane (1929-33) concerning its possible function
as a statokinetic receptor
.
As in monogononts, the stomach wall of Seison
is made of cells with microvilli
. No cilia are ap-
parent in the lumen of the digestive apparatus
: the
esophagus is lined with cuticle and has an outer
muscular sheath
. The intestine is so slender that
it is difficult to see
. The cloaca of
Seison
has been
reported to possess a cuticle (Remane, 1929-33)
.
Conclusions
Seisonids share features with both bdelloids and
monogononts
. However, some important charac-
ters are peculiar to
Seison
:
obligatory amphimixis
;
endolecythal eggs
; encysted spermatozoa
; loosely
articulated trophi
; absence of copulatory organ,
vitellarium, and cilia in the digestive apparatus
;
reduced corona
; absence of resistant stages
.
Certainly, seisonids have been heavily modified
by their life style, but some characters, such as
paired retrocerebral organ, nervous system, loose
trophi pieces, absence of muscles around the
stomach, suggest that seisonids are primitive
among the Rotifera
.
Kutikova (1983) and Markevich & Kutikova
(1989) have used coronal movements and mastax
structure to reconstruct rotifers evolution, but
they did not take seisonids into account
. These
authors regard the position of the mastax (deep
in the esophagus) to be a more primitive feature,
but Remane (1929-33) considers this to be a more
evolved character
. Attempts to reconstruct rotifer
phylogeny thus far have considered seisonids to
be the most primitive group (Remane, 1929-33
;
Epp & Lewis, 1979
; Wallace and Colburn, 1989)
.
We agree with the conclusions of these authors,
but we can now add new information which sug-
gests
that
seisonids
lie
more
closely
to
monogononts than to bdelloids, as was previously
thought
.
Nevertheless, several points remain to be clar-
ified by additional studies
:
(1) fine morphology, especially of muscles
;
(2) life cycles and dependence on
Nebalia
;
(3) food and feeding behaviors
;
(4) mating and fertilization
;
(5) ovogenesis and spermatogenesis
.

Acknowledgements
Museo di Storia Naturale of Venice, especially
Paolo Cesari, Lorenzo Bonometto and Luca
Mizzan, assisted us in locating and sampling
specimens of
S
. nebaliae
. Alois
Herzig, Fernando
Dini, Flegra Bentivegna, Salvatore Carfi gave us
invaluable help in finding older literature
. Walter
Koste permitted us to access his beautiful draw-
ings of
S
. annulatus
and provided many useful
personal observations
. Marco Ferraguti helped
us with TEM observations, made suggestions
about the manuscript, and provided useful refer-
ences
. Umberto Fascio helped us with some pic-
tures
. Last, but not least, invaluable help was
provided by Bob Wallace who provided sugges-
tions and comments on the first draft of the paper
.
Financial support was provided by a CNR grant
to C .R . and G
.M
.
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