Acta Protozool. (2007) 46: 289–309
Acta
Protozoologica
The Morphology of Three Marine Heterotrichous Ciliates, Condylostentor
auriculatus (Kahl, 1932) Jankowski, 1978, Condylostoma minutum
Bullington, 1940 and C. spatiosum Ozaki & Yagiu in Yagiu, 1944 (Ciliophora:
Heterotrichida)
Xiangrui CHEN1, Weibo SONG1, Khaled A. S. AL-RASHEID2, Alan WARREN3, Hongan LONG1,
Chen SHAO1, Saleh A. AL-FARRAJ2, Jun GONG4 and Xiaozhong HU1
Laboratory of Protozoology, Ocean University of China, Qingdao, China; 2Zoology Department, King Saud University, Saudi
Arabia; 3Department of Zoology, Natural History Museum, London, UK; 4College of Life Science, South China Normal University,
Guangzhou, China
1
Summary. The living morphology and infraciliature of three heterotrichous ciliates from the north China sea, Condylostentor auriculatus
(Kahl, 1932) Jankowski, 1978, Condylostoma minutum Bullington, 1940 and C. spatiosum Ozaki and Yagiu in Yagiu, 1944, were investigated using protargol impregnation and in vivo observations. Based on the Qingdao population, an improved diagnosis of the poorly
defined Condylostentor Jankowski, 1978 is suggested: free-swimming Stentoridae with deep, prominent vestibular cavity, apical boarder
with conspicuous ventral groove; ciliature in Stentor-like pattern, i.e. ventral suture and contrast zone of somatic kineties present; adoral
zone almost closed but interrupted on ventral side by a deep cleft, vestibulum kineties on vestibular cavity wall; paroral membrane present.
A redescription of Condylostentor auriculatus, the type species, is also supplied. Condylostoma minutum is investigated for the first time
using silver impregnation and an improved diagnosis is given based on three populations. New information about some details of the oral
apparatus is supplied for a third species, Condylostoma spatiosum.
Key words: Marine ciliates, Heterotrichea, infraciliature, morphology, taxonomy.
INTRODUCTION
Most heterotrichous ciliates are large, conspicuous
and cosmopolitan. Many forms, however, are very similar to one another when observed in vivo and few life
Address for correspondence: Weibo Song, Laboratory of Protozoology, Ocean University of China, Qingdao 266003, China; E-mail:
[email protected]
characters can be used for species separation. Furthermore the infraciliature of many nominal species remains
unknown thus the identification of these organisms
is often difficult (Dragesco 1960, 1966; Borror 1972;
Hartwig 1973; Wilbert and Kahan 1981; Dragesco and
Dragesco-Kernéis 1986; Foissner and Wölfl 1994; Petz,
Song and Wilbert 1995; Mulisch et al. 1998; Song and
Wilbert 2002; Song et al. 2003).
Kent (1881–1882) described a previously unknown
Stentor-like ciliate with a deep apical cleft and a single
290 X. Chen et al.
spherical nucleus, that he named Stentor auricula. Gruber (1884) isolated a similar organism with a moniliform macronucleus which he misidentified as Stentor
auricula. Kahl (1932) noticed this difference in the nuclear apparatus and established Gruber’s form as a new
species, S. auriculatus. Jankowski (1978) subsequently
erected the genus Condylostentor for this organism
which was assigned as the type species, although he did
not present any further information about its morphology. Hitherto, Condylostentor auriculatus has never
been examined following silver impregnation so details
of its infraciliature remained unknown.
In the present study, the poorly known Condylostentor auriculatus (Kahl, 1932) Jankowski 1978 and two
species of Condylostoma (C. minutum and C. spatiosum) isolated from coastal waters off Qingdao, China,
are investigated and redescribed. An improved diagnosis for Condylostentor is also supplied.
MATERIALS AND METHODS
Condylostentor auriculatus. Two populations were sampled
(26 June 2003 and 13 May 2005) from scallop-farming waters near
Qingdao (36°08′N, 120°43′E). The salinity was about 31‰.
Condylostoma minutum. Three populations were collected
from coastal waters of the Yellow Sea and Bohai Sea, north China:
one population was collected on 5 November 2005 from a sandy
beach near Qingdao (salinity about 17‰); a second population was
collected from coastal waters off Qingdao (salinity about 31‰);
a third population was collected from a sandy beach near Yantai
(36°16′N, 119°34′E) (salinity about 31‰).
Condylostoma spatiosum. One population was collected on 24
May 2004 from Jiaozhou Bay off Qingdao (salinity about 31‰).
Counts and measurements of stained specimens were performed
at a magnification of 1250 ×. Drawings were made with the help of
camera lucida. Terminology and systematics are according to Corliss (1979), Foissner and Wölfl (1994), and Hausmann et al. (2003).
For clarity the term contrast zone is explained here. The contrast
zone is the ventral area where the most widely spaced ciliary rows
meet the most narrowly spaced rows and where the oral primordium
appears (see Fig. 2A). This arrangement is also typically seen in
most (if not all) Stentor spp.
Deposition of slides. Voucher slides with protargol-stained
specimens were deposited in the Natural History Museum, London, UK with the following registration numbers: Condylostentor
auriculatus – 2007:5:18:1; Condylostoma minutum – 2007:5:18:2;
Condylostoma spatiosum – 2007:5:18:3 and 2005:3:24:4.
RESULTS
Redefinition of the genus Condylostentor Jankowski,
1978
The genus Condylostentor Jankowski, 1978 has
never been clearly defined, the original description
simply mentioning that this genus possesses a “deep
peristoma.” Based on the present study, we supply an
improved diagnosis for Condylostentor.
Improved diagnosis: Slightly contractile, free-swimming Stentoridae; vestibular cavity deep and prominent,
apical border with conspicuous ventral groove; ciliature
in Stentor-like pattern, i.e. ventral suture and contrast
zone of somatic kineties present; adoral zone almost
closed, interrupted on ventral side by a deep cleft; vestibulum kineties and paroral membrane present.
Comparison with related genera: In terms of body
shape and infraciliature at least four genera should be
compared with Condylostentor, i.e., Stentor, Heterostentor, Condylostoma and Maristentor (Fauré-Fremiet
1936, Bullington 1940, Tartar 1961, Jankowski 1978,
Foissner and Wölfl 1994, Lobban et al. 2002, Song and
Wilbert 2002, Song et al. 2003). Condylostentor differs
from the closely related Stentor in the following combination of characters: (1) the presence of a deeply sunk
and prominent vestibular cavity (vs. vestibular cavity
relatively inconspicuous in Stentor); (2) a conspicuous
ventral groove at the apical border (vs. ventral groove
absent in Stentor); (3) the vestibulum kineties are located on the upper wall only, not in the central area or the
bottom of the vestibular cavity (vs. kineties located in
a concentric pattern throughout the peristomial area in
Stentor) (Tartar 1961, Dragesco and Dragesco-Kernéis
1986, Foissner et al. 1992, Foissner and Wölfl 1994).
Although Foissner and Wölfl (1994) synonymized
Condylostentor with the well-known genus Condylostoma, we believe that the two can be separated by their
general morphology, especially that of the buccal apparatus. The former has: (1) a nearly closed AZM (vs.
AZM only along the left side of the buccal cavity in
Condylostoma); (2) a paroral membrane that is parallel
to the AZM and relatively inconspicuous (vs. paroral
membrane extremely well-developed and lies along
the right side of the buccal cavity in Condylostoma);
(3) many vestibulum kineties on the upper wall of the
vestibular cavity (vs. vestibulum kineties absent from
buccal cavity in Condylostoma) (Kahl 1932, Dragesco
1960, Song and Wilbert 2002, Song et al. 2003).
Morphology of Three Marine Heterotrichous Ciliates 291
Heterostentor Song and Wilbert, 2002 is also a freeliving, Stentor-like taxon but has so far only been reported from the Antarctic area. It is characterized by the
absence of a paroral membrane and in lacking a deep
vestibular cavity, both of which are present in Condylostentor (Song and Wilbert 2002).
Maristentor Lobban et al., 2002 is very similar to
Stentor and so far has only been reported from marine
habitats. Condylostentor differs from Maristentor in
having a conspicuous paroral membrane (vs. inconspicuous in Maristentor) and lacking peristomial cilia
in the central area of the vestibular cavity (vs. peristomial cilia present in these areas in Maristentor) (Lobban et al. 2002).
Condylostentor auriculatus (Kahl, 1932) (Figs 1–7;
Tables 1, 2)
Stentor auricula Gruber, 1884
Stentor auriculatus Kahl, 1932
Hitherto no data on the infraciliature were available
for this species even though it has been reported sev-
eral times (Kent 1881, Gruber 1884, Kahl 1932, FauréFremiet 1936, Bullington 1940, Ozaki and Yagiu 1941,
Foissner and Wölfl 1994). Hence, an improved diagnosis is presented based on data both from previous studies and on the present study that includes details of the
infraciliature.
Improved diagnosis for Condylostentor auriculatus: Marine colourless Condylostentor with inverted
campanulate body shape; about 200–350 µm long in
vivo; vestibular cavity with U-shaped ventral cleft;
about 140–230 membranelles in adoral zone; ca 19–28
vestibulum kineties along upper cavity wall; one clearly differentiated paroral membrane; about 100 somatic
kineties in mid-body; macronucleus moniliform with
17–34 nodules forming a J-shape.
Description of the Qingdao populations: Body
usually about 250 µm long in vivo, length: width ratio
about 2:1, variable in shape but generally conical, campanulate, trumpet-shaped, or even T-shaped in some
slender forms (Figs 1E–G). Anterior area sometimes
greatly broadened with a thick marginal rim forming
Table 1. Morphometric characterization of two populations of Condylostentor auriculatus (first line – population 1; second line – population
2). Data based on protargol-impregnated specimens. Measurements in µm (CV – coefficient of variation in %; Mean – arithmetic mean; Max
– maximum; Min – minimum; n – number of specimens examined; SD – standard deviation).
Character
Min
Max
Mean
SD
CV
n
Body length
128
256
195.7
39.4
20.1
21
170
280
227.3
35.4
15.6
15
104
160
131.9
17. 7
13.4
21
130
215
173.3
23.5
13.6
15
17
30
22.0
2.9
13.3
21
18
34
25.5
4.3
16.6
15
5
20
13.1
3.6
27.1
32
12
30
19.8
5.3
26.7
15
5
16
10.5
2.9
27.4
32
8
20
13.5
3.6
27.5
15
140
210
174.2
17.3
9.9
19
160
227
195.3
18.8
9.7
15
80
94
87.3
5.3
6.0
20
82
120
98.5
12.1
12.3
15
19
28
22.5
2.5
10.9
17
13
23
19.2
2.7
13.9
15
Body width
Number of macronuclear nodules
Length of macronuclear nodules
Width of macronuclear nodules
Number of adoral membranelles
Number of somatic kineties
Number of vestibulum kineties
292 X. Chen et al.
Fig. 1. Condylostentor auriculatus from life (A–H) and after protargol impregnation (I). A. Ventral view of a typical individual, arrow
indicates the cytopharynx. B. Pellicle in anterior portion of body, showing the cortical granules. C, D. Showing the cortical granules in
mid- and posterior portions of body. E–G. Lateral views of four specimens, arrows mark the vestibular cavity. H. Ventral view of a slender
individual, arrow indicates the longitudinal striations. I. General view, to show the nuclear apparatus. AZM – adoral zone of membranelles;
Ma – macronucleus; OP – oral primordium; SK – somatic kineties. Scale bars: 100 µm (A), 80 µm (H, I).
a deeply excavate vestibular cavity (Figs 1A, E–G arrows; 4A, B), interrupted by deep groove on ventral
side that leads into a well-defined cytopharynx (Fig.
1A, arrow). Posterior end narrowed or slightly pointed
(Figs 1E–G).
Body densely ciliated, cilia being arranged along
fine, longitudinally oriented striations (Figs 1H; 4C, D).
Pellicle furnished with numerous dark-gray, ellipsoidal cortical granules, about 1–1.5 µm long, distributed
between ciliary rows (Figs 1B–D; 4F–H). Cytoplasm
Morphology of Three Marine Heterotrichous Ciliates 293
Fig. 2. Condylostentor auriculatus after protargol impregnation. A, B. Ventral and dorsal views of the same specimen, to show the infraciliature and macronucleus; arrowheads in A mark the suture; arrows indicate the bottom of vestibular cavity. The oval area in A delineates
the contrast zone. C. Buccal apparatus, arrowheads and arrow indicate the distal and proximal ends respectively of the vestibulum kineties.
AZM – adoral zone of membranelles; PM – paroral membrane; VK – vestibulum kineties. Scale bar: 50 µm.
294 X. Chen et al.
Fig. 3. Condylostentor auriculatus after protargol impregnation. A. Buccal apparatus, arrow marks the distal end of the AZM, arrowhead
indicates the distal end of the paroral membrane, double-arrowhead marks the proximal end of the AZM. B. Detail of the paroral membrane, arrow indicates the portion consisting of double-kinetosomes, arrowheads mark the portion with multiple-kinetosomes. C. Apical view, showing the infraciliature of buccal area. AZM – adoral zone of membranelles Ma – macronucleus; PM – paroral membrane;
VK – vestibulum kineties.
colourless or slightly grayish, often appearing opaque
due to thickness of cell and numerous inclusions. Food
vacuoles often contain diatoms (Figs 1A, E, F; 4A–D).
No contractile vacuole observed. Macronucleus moniliform, usually with 17–34 nodules, and curves in anterior
region forming a J-shape (Figs 1A, H; 4B, D, I). After
protargol impregnation, nodules appear full of spherical nucleoli (Figs 5C, G). No micronuclei observed.
Cell usually attached to substratum via posterior end,
but readily detaches and swims away if disturbed. When
swimming cell rotates slowly around main body axis.
Oral apparatus as shown in Figs 1A, 2C, 3A–C and
7A–E, I. Adoral zone of membranelles (AZM) conspicuous and consists of about 200 membranelles, cilia
of which are about 30 µm in length. AZM lies along
peristomial margin and nearly closed but interrupted
on ventral side by deep cleft before entering vestibular
cavity. Within vestibular cavity AZM makes a further
one-and-half turns (Figs 1A, 3A, 7A). Bases of the
membranelles of distal portion of AZM about 10–15
µm long and significantly longer than those in proximal
portion. Each membranelle usually consists of three
Morphology of Three Marine Heterotrichous Ciliates 295
Fig. 4. Condylostentor auriculatus in vivo. A, B. Lateral views of two specimens. C. Showing an individual in contracted state, arrows indicate the longitudinal striations. D. Ventral view of a slender individual, arrows mark the moniliform macronucleus. E. To show the cilia of
the paroral membrane (PM). F–H. Details of the cortical granules in different portions of the cell: F – anterior portion, G – middle portion,
H – posterior portion. I. Macronuclear nodules. Scale bars: 150 µm.
rows of kinetosomes, two long and one very short (Figs
3A; 7C, D). Paroral membrane (PM) prominent and bipartite in structure: outer portion composed of pairs of
kinetosomes while inner part comprises closely packed
units (Figs 3A, B; 5J, K; 7I). There are about 19–28
vestibulum kineties (VK) densely arranged along upper
wall of vestibular cavity (Figs 2C; 3C; 5B, E, H, N, O;
7B, E, I), but no kineties in bottom or central areas of
vestibular cavity (Fig. 3C).
There are about 80–120 somatic kineties composed
of dikinetids as in other heterotrichous (Fig. 6E). All
kineties on dorsal side extend complete length of cell
(Figs 2B; 6B, C), while on ventral side some kineties
are shortened forming a suture (Figs 2A arrowheads;
5D, I arrows; 6D arrows). Contrast zone conspicuous
(Figs 2A, B; 6D).
Morphogenetic features: Some individuals were
observed in the process of binary division (Figs 1I;
296 X. Chen et al.
Fig. 5. Condylostentor auriculatus after protargol impregnation. A. Lateral view, to show the nuclear apparatus. B. Buccal apparatus, arrow marks the paroral membrane. C. Anterior portion of cell, arrow marks the moniliform macronucleus. D. Ventral view, arrows mark the
suture. E, F. The same portion of the buccal area (E) to show vestibulum kineties (F) to show the somatic kineties. G. Detail of the macronucleus. H. Anterior portion of buccal area, arrow indicates the vestibulum kineties. I. Detail of ventral view of cell showing the suture,
arrows mark the shortened somatic kineties. J. Buccal apparatus, arrow marks the proximal ends of vestibulum kineties which are bounded
by the paroral membrane. K. Detail of paroral membrane, arrowhead marks the inner part consisting of closely packed units of basal bodies; double arrowhead indicates the outer portion composed of pairs of kinetosomes. L. Lateral view of tail portion. M. Apical view of the
cell. N, O. Details of buccal apparatus, arrows in (N) indicate the distal ends of the vestibulum kineties, arrows in (O) mark the paroral
membrane. Scale bar: 100 µm.
Morphology of Three Marine Heterotrichous Ciliates 297
Fig. 6. Condylostentor auriculatus after protargol impregnation. A, B. Lateral and dorsal views of two cells, showing the infraciliature and
macronucleus. C, D. Dorsal and ventral views of the same specimen, arrows in (D) indicate the shortened somatic kineties. E. Somatic
kineties, arrow indicates the dikinetids. F, G. Dorsal (F) and ventral (G) views of the posterior portion of the same cell, arrows in (G) mark
the shortened somatic kineties. H. Apical view, showing the spiral buccal apparatus, arrow indicates the macronucleus. I–K. Morphogenetic
stages, (I) to show the newly formed oral primordium (arrows); (J) showing a slightly later stage of division; (K) to show a late divider,
arrows indicate the band-like macronucleus. Scale bars: 15 µm (I), 30 µm (F), 100 µm (A, C), 150 µm (K).
298 X. Chen et al.
Fig. 7. Condylostentor auriculatus after protargol impregnation. A, B. Ventral and lateral views of the anterior portion of two cells, arrow in
(A) indicates the AZM, double-arrowhead in (A) marks the proximal end of AZM, arrow in (B) indicates the vestibulum kineties, doublearrowhead marks the paroral membrane. C. Detail of AZM, arrow indicates the shortest kinety row in a membranelle. D. Proximal end of
AZM, arrows indicate the shortest rows of membranelles. E. Anterior portion of cell, to show vestibulum kineties (arrows). F. Macronuclear
nodules. G, H. A late divider, note the band-like macronucleus (arrows). I. Detail of buccal apparatus, arrows indicate the paroral membrane. Scale bars: 20 µm (C, D, F, H, I), 30 µm (E), 40 µm (A, B), 60 µm (G).
Morphology of Three Marine Heterotrichous Ciliates 299
6I–K; 7G, H). Examination of these specimens revealed
that the initial morphogenetic event is the appearance of
a small group of basal bodies (oral primordium, OP) on
the ventral side near the suture and that existing basal
bodies clearly do not contribute to the formation of the
primordium (Figs 1I, 6I). In the later stages, the moniliform macronucleus transforms into a band-like structure
that splits before cell division (Figs 6K; 7G, H).
Comparison with related species (Fig. 8, Table
2): With reference to its general morphology, Condylostentor auriculatus is most similar to another marine
morphospecies, Condylostoma wangi Foissner and
Wölfl, 1994 (formerly Stentor auriculatus sensu Wang,
1934). Although excellent illustrations and detailed
living descriptions of this organism were provided by
Wang (1934) (Fig. 8E), no information about its infraciliature is available. Condylostoma wangi can clearly
be separated from C. auriculatus by the possession of
endosymbiotic green algae (zoochlorellae) which render the cell dark green in vivo (vs. zoochlorellae absent
in C. auriculatus) (Wang 1934). Based on its general
morphology, Condylostoma wangi could be a species
of Condylostentor but details of its infraciliature are required before any decision can be made.
Other similar morphotypes to which Condylostentor
auriculatus should be compared include: Stentor auricula Kent, 1881, Stentor multiformis (Müller, 1786)
Ehrenberg, 1838, Stentor muelleri Ehrenberg, 1831,
Stentor caudatus Dragesco, 1970, Stentor polymorphus
(Müller, 1773) Ehrenberg, 1830, Stentor coeruleus
(Pallas, 1766) Ehrenberg, 1831, and Stentor introversus
Tartar, 1958. Of these Stentor auricula is most similar to Condylostentor auriculatus in terms of its body
shape and marine habitat, although it differs from the
latter in having a spherical (vs. moniliform) macronucleus (Kent 1881, Foissner and Wölfl 1994).
Stentor multiformis, which has been isolated from
both marine and freshwater habitats, differs from Condylostentor auriculatus in having fewer somatic kineties (34–45 vs. 80–120), a completely different (i.e.
Stentor-like) buccal apparatus, and a spherical (vs. moniliform) macronucleus.
Condylostentor auriculatus can be separated from
all other similar Stentor species by the following combination of features: living appearance in vivo, cell size,
number of somatic kineties, pattern of peristomial ciliature and habitat (Table 2).
Condylostoma minutum Bullington, 1940 (Figs 9–12;
Tables 3, 4)
The previous diagnosis of C. minutum was based
only on observations in vivo and thus does not include
details of the infraciliature. Therefore we here supply
an improved diagnosis based both on previous work
and on the present observations.
Improved diagnosis: Yellow-brownish Condylostoma 200–400 µm long in vivo; buccal cavity about
25% to 33% of body length; 90 membranelles on average in AZM; one frontal cirrus; about 30 somatic kineties; macronucleus moniliform with 9–18 nodules;
marine habitat.
Redescription: Body usually about 300 × 80 µm
in vivo, elongate with length to width ratio about 5:1,
posterior 1/4–1/3 of the body conspicuously narrowed
but not forming a tail (Figs 9A–C; 10A–C, F). Buccal
cavity prominent, usually about 25% (in some specimens up to 33%) body length (Fig. 9A, B). Pellicle
thin and furnished with ellipsoidal, dark-grey granules
(Fig. 10L, O) distributed between the ciliary rows,
these granules also being recognizable after protargolimpregnation (Fig. 11H). Cytoplasm yellow-brownish
and usually filled with numerous large food vacuoles
up to 35 µm in diameter (Figs 9A, B; 10A, F, M). Macronucleus located on right side of cell, moniliform with
9–18 nodules, (Figs 9C, H; 10C; 11D). No contractile
vacuole observed.
Somatic cilia 6–8 µm long, whereas those of adoral
membranelles and frontal cirri are about 20 µm long.
Locomotion relatively slow, mainly by gliding on bottom of Petri dish.
Twenty six to 33 longitudinal somatic kineties including several shortened ones on both ventral and
dorsal sides, each composed of densely arranged dikinetids (Figs 9G, H; 11A, I, L). Single conspicuous suture on ventral side of posterior portion of body (Figs
9G; 11A, I).
Adoral zone composed of 67–103 membranelles.
Paroral membrane highly developed, consisting of four
to five rows of kinetosomes (Fig. 9F). Usually one frontal cirrus (out of 56 individuals observed only one individual had two frontal cirri) with conspicuously elongate base, located near distal end of AZM and, when
two are present, they are arranged longitudinally with
a conspicuous gap between them (Figs 9F, G; 11G, J).
*
–
18–20
Number of peristomial cili- 13–28
ary rows
Number
nodules
dark gray
brown-grayish
slightly
absent
marine
present study
Colour of cortical granules
Cell colour
Contractility
Contractile vacuole
Habitat
Data source
Called Condylostoma wangi Foissner & Wölfl, 1994.
moniliform
Shape of macronucleus
macronuclear 17–34
–
Number of membranelles in 140–227
AZM
of
–
80–120
Number of somatic kineties
Wang, 1934
marine
absent
slightly
dark-green
–
moniliform
ca 300
230–270
Cell length (µm) in vivo
C. wangi*
C. auriculatus
Character
present
slightly
bluish
blue
spherical
freshwater
present
slightly
–
–
moniliform
13–21
ca 67
freshwater
present
highly
bluish
blue-greenish
moniliform
6–20
20–30
freshwater
present
highly
–
–
moniliform
–
–
–
–
450–580
S. introversus
Foissner et al., Foissner et al., Tartar, 1961
1992
1992
freshwater
present
highly
green
colourless
moniliform
5–20
ca 50
ca 200
ca 160
ca 150
55–100
ca 100
78–90
S. coeruleus
ca 4000
S. polymorphus
ca 2000
450–1000
S. caudatus
Foissner et al., Foissner et al., Dragesco, 1970
1992
1992
freshwater and freshwater
marine
present
highly
brownish
brownish
moniliform
1
6–9
ca 10
10–20
100–150
34–45
200–500
S. multiformis
–
30–50
500–1000
S. muelleri
Table 2. Morphological comparison of Condylostentor auriculatus and some closely related morphotypes of Condylostentor and Stentor.
300 X. Chen et al.
Morphology of Three Marine Heterotrichous Ciliates 301
Fig. 8. A–D – Condylostentor auriculatus (A, from Kahl, 1932; B, from Fauré-Fremiet, 1936; C, from Ozaki & Yagiu, 1941; D, from
Bullington, 1940); E – Condylostoma wangi Foissner & Wölfl, 1992 (from Wang, 1934, called Stentor auriculatus); F – Stentor muelleri
Ehrenberg, 1831 (from Kahl, 1932); G – Stentor introversus Tartar, 1958 extended and contracted (from Tartar, 1958); H – Stentor coeruleus
(Pallas, 1766) Ehrenberg, 1831 (from Dragesco & Dragesco-Kernéis, 1986); I – Stentor caudatus Dragesco, 1970 (from Dragesco, 1970);
J – Stentor polymorphus (Müller, 1773) Ehrenberg, 1830 (from Dragesco & Dragesco-Kernéis, 1986); K – Stentor multiformis (Müller,
1786) Ehrenberg, 1838 (from Packroff & Wilbert, 1991). Scale bars: 100 µm (A–E, K), 200 µm (F, G, I), 400 µm (J), 500 µm (H).
Remarks: Condylostoma minutum was first described by Bullington (1940) since when there has been
no redescription. The Qingdao and Yantai populations
both correspond well with the original description in
terms of the general morphology, body size and shape
and habitat (Fig. 12A; Table 4).
302 X. Chen et al.
Table 3. Morphometric characterization of three populations of Condylostoma minutum. Data based on protargol-impregnated specimens.
Measurements in µm.
Character
Min
Max
Body length
208
360
150
Body width
Length of buccal cavity
Number of somatic kineties
Number of adoral membranelles
Number of frontal cirri
Number of macronuclear nodules
Length of macronuclear nodules
Width of macronuclear nodules
SD
CV
n
274.5
44.4
16.2
21
240
191.0
25.1
13.1
20
130
250
190.1
35.6
18.8
15
88
156
120.2
17.1
14.3
21
65
110
85.3
10.1
11.8
20
70
95
81.3
8.6
10.5
15
44
88
64.1
11.4
17.8
21
50
80
60.5
8.3
13.6
20
58
87
69.2
7.7
11.2
15
28
33
30.7
1.3
4.2
22
26
31
30.0
1.2
3.8
20
28
33
30.7
1.2
4.0
15
80
94
88.1
3.7
4.2
19
67
86
76.5
5.6
7.3
20
75
103
90.9
7.4
8.1
15
1
2
1.1
0.2
20.0
21
1
1
1
0
0
20
1
1
1
0
0
15
10
15
12.4
1.2
9.9
20
11
16
12.5
1.4
10.9
20
9
18
13.7
2.4
17.8
15
12
40
21.7
6.7
31.2
23
5
27
16.5
6.3
38.2
20
12
20
15.6
2.5
16.2
15
10
20
13.5
2.9
21.6
23
4
12
9.0
1.9
20.7
20
6
12
9.0
1.7
19.2
15
Within the genus Condylostoma there are six marine
morphotypes that should be compared with Condylostoma minutum: C. magnum Spiegel, 1926, C. spatiosum Ozaki and Yagiu, 1944, C. curva Burkovsky, 1970,
C. granulosum Bullington, 1940, C. magnum (sensu
Mean
Wilbert and Song 2005) and C. arenarium Spiegel,
1926. Of these, Condylostoma minutum is most similar to C. magnum and C. spatiosum in terms of body
shape and the general appearance of the buccal area.
However, C. minutum can be separated from the latter
Morphology of Three Marine Heterotrichous Ciliates 303
Fig. 9. Condylostoma minutum from life (A–C, E) and after protargol impregnation (D, F–H). A, B. General view of two typical individuals. C. To show different body shapes and the moniliform macronucleus. D, E. To show cortical granules. F. Ventral view of anterior portion
of cell, arrows mark the paroral membrane, double-arrowhead indicates the frontal cirrus, arrowheads show the fragmented somatic kineties. G, H. Ventral and dorsal views of the same specimen, note the prominent ventral suture (arrows), the frontal cirrus (double-arrowhead)
and the shortened somatic kineties (arrowheads). AZM – adoral zone of membranelles; PM – paroral membrane. Scale bars: 80 µm (A, B);
140 µm (G).
304 X. Chen et al.
Fig. 10. Photomicrographs of Condylostoma minutum from life. A–D, F. Ventral views, to show different body shapes; arrows in D mark
the AZM. E, G, I, N. Ventral view of anterior portion of the cell to indicate the buccal region; note the paroral membrane (arrows in E, I, N)
and the frontal cirrus (arrowhead in N). H, K. Posterior region of cell, note the conspicuous ventral sutures. J. To show the inclusions in the
food vacuoles. L, O. Cortical granules. M. Arrowheads mark the moniliform macronucleus. Scale bars: 80 µm (A, B, C, F).
Spiegel, 1926
Wilbert and
Song, 2005
Song et al.,
2003
* Sensu Wilbert and Song (2005).
** About 250 µm long based on protargol-impregnated specimens.
*** About 1/6 in protargol-impregnated specimens.
– Data unavailable; AZM – adoral zone of membranelles.
Bullington,
1940
Data source
this study
Song and
Wilbert,
1997
Shao et al.,
2006
Petz et al.,
1995
ca 1/5
***
ca 1/3
1/3–2/5
1/4–1/3
ca 1/4
ca 1/4
Length of buccal field to cell length in vivo
1/4–1/3
–
> 120
123–210
68–108
113–153
150–200
–
Number of membranelles in AZM
67–103
14–16
ca 10
6–13
5–13
13–22
10–15
ca 13
Number of macronuclear nodules
12–19
ca 30
28–65
22–32
51–63
26–33
ca 32–40
Number of somatic kineties
47–56
1–2
–
Number of frontal cirri
2
2
4–8
1–3
2 or more
ca 30
400–600
**
590–2140
150–350
400–700
400–800
199–264
Cell length (µm) in vivo
200–400
C. spatiosum
C. magnum
C. minutum
C. minutum
Character
Table 4. Morphological comparison of some closely related morphotypes in the genus Condylostoma.
C. curva
C. granulosum
C. magnum*
C. arenarium
Morphology of Three Marine Heterotrichous Ciliates 305
two species by having fewer somatic kineties (26–33
vs. 47–56 in C. magnum, 51–63 in C. spatiosum), usually one frontal cirrus (vs. two in both C. minutum and
C. spatiosum), fewer adoral membranelles (67–103 vs.
ca 150–200 in C. magnum, 113–153 in C. spatiosum)
and a smaller body size in vivo (200–400 µm vs. 400–
800 µm in C. magnum, 400–700 µm in C. spatiosum)
(Song and Wilbert 1997, Shao et al. 2006) (Figs 12A–
C, H–J; Table 4).
Condylostoma minutum should also be compared
with Condylostoma magnum (sensu Wilbert and Song
2005) which was found in fixed samples isolated from
the Antarctic area (Wilbert and Song 2005). Since
no live observations were made of this population of
C. magnum a detailed comparison is difficult to perform. However, based on impregnated specimens,
C. minutum has a conspicuously more prominent buccal cavity (25% to 33% of body length vs. about 15% in
C. magnum) and fewer adoral membranelles (67–103
vs. > 120 in C. magnum) (Fig. 12F; Table 4).
Condylostoma minutum appears to be similar to the
poorly known C. arenarium Spiegel 1926, which has
never been described using modern methods and hence
its infraciliature remains unknown. Based on observations in vivo, however, Condylostoma minutum differs
from latter in its smaller size (< 400 µm vs. 400–600
µm in C. arenarium) and more conspicuous buccal cavity (25% to 33% of body length vs. about 20% body
length in C. arenarium) (Table 4; Spiegel 1926).
Condylostoma curva also closely resembles
C. minutum in terms of its general morphology (Song
et al. 2003). Nevertheless, the latter has a smaller buccal cavity (25% to 33% of body length vs. 33% to 40%
of body length in C. curva), a plumper body shape and
fewer frontal cirri (1–2 vs. 4–8 in C. curva) (Figs 12D,
K; Table 4).
Condylostoma minutum differs from C. granulosum,
another morphologically similar species, in having
a much smaller body size (200–400 µm vs. 590–2140
µm in C. granulosum), fewer adoral membranelles (67–
103 vs. ca 123–210 in C. granulosum), a more slender
body shape with narrowed posterior end (vs. ellipsoidal
with rounded posterior end in C. granulosum) and a relatively shorter buccal cavity (usually < 33% of body
length vs. usually > 33% of body length in C. granulosum) (Figs 12E, L; Table 4; Petz et al. 1995).
306 X. Chen et al.
Fig. 11. Photomicrographs of Condylostoma minutum Bullington, 1940 (A, D–L) and C. magnum Spiegel, 1926 (B, C, from Song and Wilbert 1997) after protargol impregnation. A, F. Ventral and dorsal views of the same specimen, note the conspicuous ventral suture (arrows
in A). B, C. Buccal apparatus, to show the frontal cirrus/cirri (arrowheads in B, C) and the cirrus-like anterior end of paroral membrane
(arrow in B). D. Ventral view, to show the moniliform macronucleus. E. Anterior portion of cell, arrow marks the paroral membrane. G, J.
Buccal apparatus, arrows mark the frontal cirrus/cirri. H. Cortical granules. I, L. Caudal portion of cell, to show the ventral suture (arrows).
K. Food vacuole inclusions. Scale bar: 50 µm (A).
A note on Condylostoma spatiosum Ozaki & Yagiu in
Yagiu, 1944 (Figs 12C, J; 13)
A Qingdao population of C. spatiosum was recently
described in detail by Shao et al. (2006) therefore a full
redescription is unnecessary. However, one structure,
i.e. the left frontal cirri, was misinterpreted by Shao et
al. (2006). Having carefully examined the structure of
oral apparatus of C. spatiosum we found that the pos-
Morphology of Three Marine Heterotrichous Ciliates 307
Fig. 12. A, H – Condylostoma minutum Bullington, 1940 (from Bullington 1940), B, I – C. magnum Spiegel, 1926 (from Song and Wilbert
1997); C, J – C. spatiosum Ozaki and Yagiu in Yagiu, 1944 (from Shao et al. 2006); D, K – C. curva Burkovsky, 1970 (from Song et al.
2003); E, L – C. granulosum Bullington, 1940 (from Petz et al. 1995); G – C. arenarium Spiegel, 1926 (from Spiegel 1926); F, M – C. magnum (sensu Wilbert and Song 2005) (from Wilbert and Song 2005). All arrows mark the frontal cirrus/cirri, double-arrowhead in J indicates
the anterior end of paroral membrane (see text). Scale bars: 70 µm (A), 100 µm (D, F, G), 150 µm (C), 180 µm (E), 200 µm (B).
308 X. Chen et al.
Fig. 13. Condylostoma spatiosum Ozaki and Yagiu in Yagiu, 1944 after protargol impregnation. A–E. Ventral views of the anterior end of
cell. Arrowheads mark the right frontal cirrus. Arrows indicate the left frontal cirrus which is connected posteriorly with the paroral membrane. FC1 – right frontal cirrus; FC2 – left frontal cirrus; PM – paroral membrane. Scale bar: 20 µm.
terior end of the left frontal cirrus is connected with
the anterior end of the paroral membrane (Fig. 13),
which was not clearly reported by Shao et al. (2006).
In terms of morphogenesis, the left frontal cirrus and
the paroral membrane are homologous, both structures
being formed from the paroral membrane anlage during
morphogenesis (Shao et al. 2006).
Acknowledgements. This work was supported by the “Natural
Science Foundation of China” (Project No. 40676076; 30430090),
a grant from Center of Excellence in Biodiversity, King Saud University and the Darwin Initiative Programme (Project No. 14-015)
which is funded by the UK Department for Environment, Food and
Rural Affairs.
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Received on 11th July, 2007; revised version on 26th September; accepted on 27th September, 2007