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To cite this article: Fernando Gómez, Haruyoshi Takayama, David Moreira & Purificación
López-García (2016) Unarmoured dinoflagellates with a small hyposome: Torodinium and
Lebouridinium gen. nov. for Katodinium glaucum (Gymnodiniales, Dinophyceae), European
Journal of Phycology, 51:2, 226-241, DOI: 10.1080/09670262.2015.1126767
Article views: 14
We investigated the morphology and evolutionary relationships of Torodinium spp. and Katodinium glaucum, unar-
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moured dinoflagellates characterized by a small hyposome. An emended generic description of Torodinium was
proposed based on light and scanning electron microscopy. Torodinium exhibited a unique combination of morpholo-
gical features including a minute hyposome, a long episome with longitudinal ribs and a canal of unknown function on
the dextro-lateral side. Unlike any known dinoflagellate both cingulum and sulcus extended in the episome. The apex
surface showed ribs that converged in a bill-like projection. The shape of the apical groove was a circular spiral that
extended around the apex running in 2.5 turns in an anticlockwise direction. The type species T. teredo was usually
longer than T. robustum. The longitudinal outline of T. teredo was linear, with almost parallel margins, a circular
transversal section, a relatively large hyposome and a conspicuous bill-like projection. The longitudinal outline of
T. robustum was oblong, widened in the middle, with an ellipsoidal transversal section, a small hyposome and a less
prominent bill-like projection. Several morphological features of Katodinium glaucum (=Gyrodinium glaucum)
resembled Gyrodinium, such as the cingular displacement, longitudinal ribs, trichocysts, rod-shaped and refractile
bodies and a capsule that surrounded the spherical nucleus. Distinctive features of K. glaucum were the horseshoe-
shaped apical groove under a tongue-shaped notch pointed towards the dorsal side, and a bifurcated proximal end of the
cingulum. Phylogenetic analysis revealed that Torodinium spp. and K. glaucum formed two independent lineages with
no close relationships with other known dinoflagellates. The morphology of K. glaucum was distant from the type
species of Katodinium. We propose the new genus and combination Lebouridinium glaucum gen. nov., comb. nov. for
the species Katodinium glaucum.
Key words: acrobase, apical groove, athecate Dinoflagellata, Gymnodinium, Gyrodinium, molecular phylogeny, naked
dinoflagellate, new genus, taxonomy
(1895). Apparently Kofoid & Swezy (1921) did not MATERIALS AND METHODS
observe any specimens of T. teredo. However, they Sampling and isolation of material
considered that the apex of T. teredo lacked the apical
groove (which they called reversed terminal anterior In the Mediterranean Sea, the specimens of Torodinium spp.
loop of the sulcus). This feature, together with the were collected from October 2007 to September 2008 by
slowly filtering surface seawater taken from the pier of the
relative ratio between the length and the transdia-
Station Marine d’Endoume at Marseille (43°16′48.05″N, 5°
meter, with a stouter episome in T. robustum, was
20′56.22″E, bottom depth 3 m). A strainer of 20 µm mesh
used for species distinction. size was used to collect planktonic organisms from water
The two Torodinium species have been commonly volumes ranging between 10 and 100 l, depending on particle
reported in the literature and further authors agreed concentration. The plankton concentrate was scanned in set-
with the diagnosis given by Kofoid & Swezy, with tling chambers at 100× magnification with an inverted micro-
no new taxonomic information (Elbrächter, 1979; scope (Nikon Eclipse TE200, Nikon Inc., Tokyo, Japan).
Dodge, 1982; Sournia, 1986; Hansen & Larsen, Cells were photographed alive at 200× or 400× magnification
1992; Steidinger & Tangen, 1997; Gárate-Lizárraga with a Nikon Coolpix E995 digital camera. During the sam-
& Muciño-Márquez, 2013). Gómez (2009) reported pling on 17–21 December 2007, the distinction between
that some specimens of Torodinium showed a body species was not defined and we pooled a total of 20 speci-
extension that protrudes from the hyposome and mens of Torodinium spp. into a single sample for PCR ampli-
fication and cloning (isolated cells FG21–2, FG21–3, FG21–
accumulation bodies (tentative food vacuoles).
4, GenBank accession numbers KR139781, KR139782,
These features supported the mixotrophic character KR139783). Sporadic samplings were carried out in the
of Torodinium.
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sample was slowly siphoned off with small-bore tubing over and a final elongation step of 7 min at 72ºC. A nested
6 days. The remaining 50 ml of concentrate, representing 500 PCR was then carried out using 2–5 µl of the first PCR
ml whole water, was then settled in composite settling cham- products in a GoTaq (Promega, Lyon, France) polymerase
bers. The sample was examined in Utermöhl chambers at reaction mix containing the eukaryotic-specific primers
100× magnification with a Nikon inverted microscope EK-82F (5′–GAAACTGCGAATGGCTC–3′) and EK-
(Nikon Eclipse TE200) and the specimens were photo- 1498R (5′–CACCTACGGAAACCTTGTTA–3′) (López-
graphed with a digital camera (Nikon Coolpix E995). García et al., 2001) and similar PCR conditions as
In the North Pacific Ocean, samples were collected with a described above. Negative controls without template
plankton net (30 µm mesh size) from the coastal Inland Sea of DNA were used at all amplification steps. Amplicons of
Japan at Kure (34°10′30″N, 132°33′21.6″E). The living con- the expected size (~1700 base pairs) were then sequenced
centrated samples were observed at 400× and 1000× magni- bi-directionally using primers EK-82F and EK-1498R
fication with an upright microscope (Olympus BH2), and using an automated 96-capillary ABI PRISM 3730xl
photographed with a digital camera (Canon EOS Kiss F., sequencer (BC Genomics, Takeley, UK). In other sam-
Canon Inc., Tokyo, Japan). ples, the amplified product was subsequently cloned
using the Topo TA Cloning system (Invitrogen, Life
Technologies, Saint Aubin, France) following the instruc-
Scanning electron microscopy tions provided by the manufacturers. Three clones were
picked and the corresponding insert amplified using vec-
Seawater samples were collected with a bucket from the
tor primers. Amplicons of the expected size were fully
coastal areas of the Inland Sea of Japan along Hiroshima
sequenced (Cogenics, Meylan, France) with vector pri-
Prefecture in 1980–1985 as described in Takayama (1998).
mers using the same automated sequencer.
For scanning electron microscopy, dinoflagellate cells were
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propose the separation of both species based on cell Emended generic description of Torodinium based on
length, with Torodinium teredo (55–100 µm long) scanning electron microscopy
usually longer than T. robustum (40–75 µm long),
The detailed morphology was examined from speci-
and outline of the cells. The outline of T. teredo was
mens of Torodinium spp. collected from the south of
linear, with almost parallel margins, while the outline
Japan (Figs 25–50). We first established the orienta-
of T. robustum was oblong, widened in the middle
tion of the cells, whose ventral side was defined by the
(Figs 1–24). The hyposome and the bill-like projec-
position of the sulcus and the pore of the longitudinal
tion, the latter further described in detail, were more
flagellum. The hyposome was small and conical. The
conspicuous in T. teredo than in T. robustum. From the
ventral side of the hyposome was concave and occu-
pier of the Marine Station of Endoume, some records
pied by the posterior end of the sulcus below the pore
corresponded to larger and more slender specimens in
of the longitudinal flagellum (Figs 25–28).
agreement with the definition of T. teredo (Figs 1–6).
The sulcus extended for almost the entire ventral
Other observations corresponded to shorter specimens
side of the hyposome, occupying about 1/3 of the
with an oblong shape in agreement with our definition
contour of the hyposome (Figs 28–29). The pore of
of T. robustum (Figs 7–11). One of the specimens of T.
the longitudinal flagellum was located in the sulcus
teredo showed an interesting morphological feature
between the transversal flagellar pore and the pos-
with a kind of edging of crenate margin (with rounded
terior end of the cingulum (Figs 25–30). The poster-
teeth) that extended longitudinally in the episome
ior end of the sulcus, directed posteriorly from the
(Fig. 1).
longitudinal flagellar pore, was placed in a wide
Numerous specimens were observed in Lugol-fixed
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Figs 1–24. Light microscopy (LM) images of Torodinium teredo and T. robustum. Bright field optics, except Fig. 16 by epifluor-
escence microscopy. Figs 1–11. Specimens from Endoume, Marseille, France. Figs 1–6. T. teredo. Figs 7–11. T. robustum. Fig. 12.
(continued)
Torodinium and Lebouridinium gen. nov. 231
previously reported (Fig. 28). The transdiameter sensu 53, 57). The first apical rib emerged in the dextro-
Kofoid & Swezy corresponded to the cell depth (ven- lateral side from the base of the apical groove. Each rib
tral to dorsal distance). The episome occupied about 9/ emerged at each side of the basis of the apical groove
10 of the cell length and ended in a hemispheric and converged between the sinistro-lateral and dorsal
bonnet-shaped apex (Figs 27, 35–50). The cell surface sides. The last pair of apical ribs joined in a triangular
of the episome was covered by well-marked longitu- structure (Figs 48, 53, 57).
dinal ribs. There were 12–14 longitudinal ribs (~0.35
µm wide) that were equidistant and separated by 3–4
µm (Figs 35–50). In addition to the ribs, at least on the Differences between T. teredo and T. robustum
dextro-lateral side, the episome surface was covered As reported above, under light microscopy T. ter-
in fine longitudinal striae (Fig. 36). In addition to the edo was usually longer than T. robustum. The
anterior extensions of the sulcus and cingulum, the longitudinal outline of T. teredo was linear, with
episome showed a third groove. This deep groove almost parallel margins, a circular transversal sec-
appeared in the middle of a concave area on the tion, a relatively large hyposome and a conspicu-
dextro-lateral side (Figs 33, 35, 38, 41). This concave ous bill-like projection. The longitudinal outline of
area was not observed in live cells and it could not be T. robustum was oblong, widened in the middle,
ruled out that the depression of the deep groove was with an ellipsoidal transversal section, a small
due to a sample preparation artefact. The anterior and hyposome and a less prominent bill-like projec-
posterior ends of this groove were different (Figs 33, tion. Based on SEM, the transversal section was
35). The anterior one ended in a straight line between circular (Figs 53–54) and ellipsoidal (Figs 57–58)
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two longitudinal ribs that converged at their anterior in T. teredo and T. robustum, respectively.
ends (Fig. 35). The posterior end of the groove was Torodinium teredo (Figs 27–29, 46–47, 51–52,
located above the distal end of the anterior cingulum 54) showed a larger hyposome than T. robustum
and showed a short loop towards the left side (Figs 28–34, 35, 38, 41, 55–56, 58). In T. teredo,
(Figs 28–33, 35). We were unable to find an analogous the proximal part of the anterior extension of the
structure in any other dinoflagellate. This straight deep sulcus and cingulum extended transversally
groove was named a ‘slender canal, anterior pusule’ towards the dextral side and then described a
by Kofoid & Swezy (1921, p. 391). Following this marked loop (Figs 52, 54). In contrast, in T. robus-
terminology, we named this groove the lateral canal. tum the proximal part of the anterior extension of
The hemispherical apex showed unique morpholo- the sulcus and cingulum extended obliquely
gical structures such as a spiral-shaped apical groove towards the episome (Figs 55, 58). The anterior
and ribs that converged in a pointed projection extension of the sulcus and cingulum was more
(Figs 37–50). The posterior end of the apical groove displaced towards the dextral side in T. teredo than
began above the anterior end of the sulcus (Figs 39, in T. robustum (Figs 52, 54, 55, 58). Consequently,
55, 58). The apical groove continued below the basis the proximal part of the anterior extension of the
of the pointed projection and took 2.5 turns describing cingulum and sulcus were visible in ventral view
an anticlockwise spiral that ended in the dextro-lateral in T. robustum (Fig. 55) and in dorsal view in T.
side, pointing to the lateral canal in T. teredo (Figs 42– teredo (Fig. 52). In the apex of T. teredo, the bill-
45, 53). like projection was more conspicuous, overlying
The hemispherical apex showed a pointed projec- the episome, and oriented between the ventral
tion oriented towards the sinistro-lateral or dorsal and sinistro-lateral sides (Figs 45–50, 53). The
sides in T. teredo and T. robustum, respectively bill-like projection of T. robustum was more
(Figs 27, 42–50, 53, 57). This structure was here reduced, and oriented between the sinistro-lateral
named ‘bill-like projection’. Six or seven ribs coming and dorsal sides (Figs 40–41, 57).
from the basis of the apical groove converged from
each side into the bill-like projection (Figs 27, 42–50).
These transversal or oblique apical ribs were thinner Morphology of Katodinium glaucum
and they were not connected with the prominent long- Cells were spindle-shaped, tapering at both the apex
itudinal ribs on the episome. The most posterior apical and the antapex, and about 35–40 µm long and
rib was placed above the apical groove (Figs 48–50, about 14–22 µm wide (Figs 59–63). The cells
Figs 1–24. Continued
Lugol-fixed specimen of T. robustum from the open Algerian Basin, western Mediterranean Sea (BOUM cruise, station #21). The
arrow points to the body extension. Fig. 13. T. robustum from the Gulf of Lions, isolated cell #FG187 (GenBank accession number
KR139784). Figs 14–16. T. teredo from Gulf of Lions. Note the chloroplasts in epifluorescence microscopy. Fig. 17. T. robustum
from Banyuls-sur-Mer. The arrow points to the longitudinal flagellum. Fig. 18. Torodinium sp. from the Bay of Villefranche-sur-Mer,
France. Figs 19–23. T. robustum from the port of Valencia, Spain. The arrows point to the longitudinal ribs. Fig. 24. T. teredo from the
port of Valencia. The arrow indicates the apical groove. ag = apical groove. bp = bill-like projection. lf = longitudinal flagellum. lr =
longitudinal rib. Scale bars: 10 µm.
F. Gómez et al. 232
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Figs 25–34. Scanning electron microscopy (SEM) images focused on the hyposome of five specimens of Torodinium. Figs 25–27.
Three specimens of T. teredo. Figs 28–34. Two specimens of T. robustum. The micrographs 29–34 correspond to the same specimen
(also Figs 36–44). Fig. 25. Ventral view. Fig. 26. Ventro-antapical view. Fig. 27. Ventral view. Fig. 28. Antapical view. Fig. 29.
Ventro-antapical view. Figs 30–31. Ventral view. Fig. 32. Dorsal view. Fig. 33. Dextro-lateral view. Fig. 34. Ventral-dextro-lateral
view. ac = anterior cingulum. as = anterior sulcus. bp = bill-like projection. ci = cingulum. lc = lateral canal. lf = longitudinal
flagellum. lfp = longitudinal flagellar pore. sl = sulcal lip. su = sulcus. tf = transversal flagellum. tfp = transversal flagellum pore. Scale
bar: 5 µm.
Torodinium and Lebouridinium gen. nov. 233
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Figs 35–50. SEM focused on the hyposome of five specimens of Torodinium. Figs 35–44. T. robustum. Micrographs 35–43
correspond to the same specimen (also Figs 29–34). Figs 44–50. T. teredo. Fig. 35. Dextro-lateral view. Fig. 36. The arrows point
to the longitudinal striae. Fig. 37. Apex. Fig. 38. Ventral view. Fig. 39. Apex. Figs 40–41. Dextro-lateral dorsal view. Figs 42–43.
Apex. Fig. 44. Another specimen of T. robustum in apical view. Fig. 45. T. teredo in apical-dorsal view. Figs 46–48. Another
specimen in dorsal view. Fig. 49. Another specimen in sinistro-lateral view. Fig. 50. Dorsal view. ag = apical groove. ar = apical rib. as
= anterior sulcus. bp = bill-like projection. lc = lateral canal. lr = longitudinal rib. sl = sulcal lip. su = sulcus. Scale bar: 5 µm.
under division reached 55–60 µm long (Figs 64–66). in the upper episome (Figs 59–62). Groups of tri-
The hyposome was about 1/4 of the cell length. The chocysts and some rod-shaped bodies were situated
descending cingulum was displaced by three to four along the cell margin in the episome and the hypo-
cingular widths (Figs 59–63). Cells lacked chloro- some (Figs 60–61). The nucleus was spherical and
plasts. Vacuoles and refractile bodies were observed located in the posterior part of the episome at the
F. Gómez et al. 234
51 52 53 55 56 57
lc
ag lc
bp
as
bp ac ag
sl ac
as
ac
sl as
su
as su
ci ci
ac lc
lc
54 58
ac lc
as
lc
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Figs 51–58. Line drawings of different views of Torodinium teredo (Figs 51–54) and T. robustum (Figs 55–58). Figs 51, 55. Ventral
view. Figs 52, 56. Dorsal view. Figs 53, 57. Apical view. Figs 54, 58. Antapical view. ac = anterior cingulum. ag = apical groove; as =
anterior sulcus. bp = bill-like projection. ci = cingulum. lc = lateral canal. sl = sulcal lip. su = sulcus.
Figs 59–74. LM (Figs 59–65) and SEM (Figs 66–74) images of Katodinium glaucum from South Japan. Fig. 59. Specimen with a
large vacuole. Figs 60–61. Another specimen. Note the capsule of the nucleus, the rod-shaped bodies, refractile bodies and
trichocysts. Figs 62–63. Another specimen. Note the longitudinal ribs and the bifurcation of the proximal end of the cingulum,
named anterior cingular extension. Figs 64–66. Specimen undergoing binary division. Fig. 67. Ventral view. Fig. 68. Dextro-lateral
view. Fig. 69. Dorsal-apical view. Fig. 70. Ventral view. Figs 71–72. Sinistro-lateral and ventral view. The inset shows the proximal
end of the cingulum. Figs 73–74. Detail of the apex. ac = anterior extension of the cingulum. ag = apical groove. ci = cingulum. lf =
longitudinal flagellum. lr = longitudinal rib. n = nucleus. rb = refractile body. rsb = rod-shaped body. su = sulcus. tf = transversal
flagellum. tr = trichocyst. v = food vacuole. Scale bars: 10 µm.
F. Gómez et al. 236
Fig. 78. Bayesian phylogenetic tree of dinoflagellate SSU rDNA sequences, based on 1584 aligned positions. Names in bold
represent sequences obtained in this study. Numbers at nodes are posterior probabilities (values <0.50 are omitted). The scale bar
represents the number of substitutions for a unit branch length.
Torodinium and Lebouridinium gen. nov. 237
Rh
79 80 82 83 84
sulc. rod.
c
Cp gir. epi.
pus. rod.
81 n.
sulc.
gir. hyp.
gir.
qG tr. fl.
qF hyp.
long. fl.
gir.
hyp.
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85 86 87 88 89 90
Figs 79–90. Line drawings of Torodinium teredo and T. robustum in the literature. Fig. 79. Gymnodinium teredo redrawn from
Paulsen (1908). Figs 80–82. T. robustum redrawn from Kofoid & Swezy (1921). Fig. 80. Ventral view. Fig. 81. Dextro-lateral view.
Fig. 82. Sinistro-lateral view. Fig. 83. T. teredo redrawn from Kofoid & Swezy (1921). Fig. 84. T. robustum redrawn from Lebour
(1925). Fig. 85. T. teredo redrawn from Elbrächter (1979). Fig. 86. T. robustum redrawn from Elbrächter (1979). Fig. 87. T. robustum
redrawn from Dodge (1982). Fig. 88. T. robustum redrawn from Sournia (1986). Fig. 89. T. robustum redrawn from Hansen & Larsen
(1992). Fig. 90. T. teredo redrawn from Steidinger & Tangen (1997).
Kofoid & Swezy (1921) reported also that both specimens showed scarce pigmentation (Figs 2, 6,
species of Torodinium lacked striae on the cell 25), while it was greenish in others (Fig. 18). The
surface. However, the surface of the episome is first micrograph of Torodinium under epifluores-
covered with prominent longitudinal ribs as is cence microscopy showed a specimen with few
even revealed by light microscopy (Fig. 23). long longitudinal plastids restricted to the ventral
Some micrographs in the literature also showed side of the cell (Fig. 16).
the ribs in the episome (Sournia, 1986; Gárate- The occurrence of three grooves in the episome
Lizárraga & Muciño-Márquez, 2013). The pigmen- of Torodinium was not reported in previous stu-
tation of Torodinium is another controversial mat- dies. The anterior extension of the cingulum is
ter. Elbrächter (1979) reported that the chloroplasts short and it very probably went unnoticed in
were greenish-yellow to pale brown for T. teredo, studies based on light microscopy. An anterior
and brown for T. robustum. In contrast, Steidinger extension of the cingulum has been reported in
& Tangen (1997) reported that the pigmentation some species of Gymnodinium, Cochlodinium F.
was brown and green for T. teredo and T. robus- Schütt and Warnowia Lindemann (Takayama,
tum, respectively. In our observations, some 1985, 1998). To the best of our knowledge,
Torodinium and Lebouridinium gen. nov. 239
91 92 93 94 95
96 97
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98 99 100
Figs 91–100. Line drawings of Katodinium nieuportense, Lebouridinium glaucum, Gymnodinium vestificii and Amphidinium
extensum. Fig. 91. Katodinium nieuportense redrawn from Conrad (1926). Fig. 92. Spirodinium glaucum redrawn from Lebour
(1917). Fig. 93. Gyrodinium glaucum redrawn from Lebour (1925). Fig. 94. G. glaucum redrawn from Kofoid & Swezy (1921).
Fig. 95. K. glaucum redrawn from Elbrächter (1979). Fig. 96. Gyrodinium glaucum redrawn from Dodge (1982). Fig. 97. K. glaucum
redrawn from Steidinger & Tangen (1997). Fig. 98. Gymnodinium vestificii redrawn from Paulsen (1908). Fig. 99. G. vestificii
redrawn from Kofoid & Swezy (1921). Fig. 100. Amphidinium extensum redrawn from Lebour (1925).
Torodinium is the only known genus with exten- Elbrächter, 1979; Dodge, 1982; Sournia, 1986).
sions of both sulcus and cingulum in the episome Kofoid & Swezy denoted the lateral canal as a
(Figs 35, 52). Another distinctive character of pusule (Fig. 63). Several functions have been attrib-
Torodinium is the sulcal lip (Figs 26–27). A ten- uted to the dinoflagellate pusule, including the
tatively analogous feature has been reported as a incorporation of particles (Klut et al., 1987). The
tube-like structure in the genus Takayama de distribution of Torodinium in oligotrophic surface
Salas, Bolch, L. Botes & Hallegr. (de Salas oceanic waters, the scarce chloroplasts, the presence
et al., 2003). of food vacuoles and the body extension suggest
Kofoid & Swezy (1921, p. 391) reported that that Torodinium is indeed able to ingest particulate
‘From the anterior flagellar pore there runs ante- matter (Gómez, 2009). We have not yet observed
riorly at the left of the nucleus a slender canal, the mechanism of prey capture and ingestion. The
the anterior pusule’. The lateral canal was erro- body extension was noticed only in specimens that
neously reported in further literature as reaching were fixed immediately after collection (Gómez,
the cingulum, reaching the anterior flagellar pore 2009; Fig. 12). During observations of live speci-
or being confused with the sulcus (Figs 64–70). mens the body extension could be retracted due to
All previous studies have illustrated the lateral manipulation stress. The projection of a body exten-
canal in contact with the cingulum (Lebour, 1925; sion from the hyposome is a feature known in other
F. Gómez et al. 240
gymnodinioid dinoflagellates (Persson et al., 2013). observed by light and scanning electron microscopy
Gymnodinioid dinoflagellates typically ingest their (Figs 63, 71–72) that the proximal end of the cingu-
prey by direct engulfment through the sulcal area in lum showed a short bifurcation or, alternatively, a
the hyposome [e.g. Gyrodinium spirale (Bergh) leftwards notch that transversally divided the cingu-
Kof. & Swezy; Hansen, 1992]. However, lum (Figs 75–76). This feature was not reported in the
Torodinium has a minute hyposome and posterior literature. The tongue-shaped notch (Figs 94–95) was
sulcus, probably insufficient for the ingestion of first reported by Takayama (1985, 1998; Fig. 97).
large prey. The lateral canal is a structure unknown
in any other dinoflagellate and its function remains
uncertain. It can be hypothesized that the body Evolutionary affinities of Lebouridinium
extension that emerged from the hyposome may The morphology of Lebouridinium glaucum is very
facilitate prey capture and the subsequent ingestion different from the type of Katodinium, K. nieupor-
through the lateral canal (Figs 33, 35). tense (Fig. 91), an insufficiently described species
The apex of Torodinium is also highly distinctive. that is only known from the original description
Schütt (1895) illustrated a group of plastids around a (Conrad, 1926). Some morphological features such
central plastid or oil globule forming a star of eight or as the cingular displacement, longitudinal ribs, tricho-
nine rays, further re-drawn by other authors (Figs 60, cysts, rod-shaped and refractile bodies and a capsule
63–65). This unusual star-shaped distribution of the that surrounded the spherical nucleus resemble the
plastids coincides with the apical ribs that form the type of Gyrodinium (Hansen & Daugbjerg, 2004;
bill-like projection (Fig. 48). In one of the earliest
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AUTHOR CONTRIBUTIONS (Dinophyceae, Pfiesteriaceae), from coastal waters off Korea: mor-
phology and molecular characterization. Harmful Algae, 41: 25–37.
F. Gómez: collection, isolation, light microscopy and drafting; Kim, K.-Y. & Kim, C.-H. (2007). Phylogenetic relationships among
H. Takayama: collection, isolation, light and electron micro- diverse dinoflagellate species occurring in coastal waters off Korea
scopy; P. López-García: molecular analysis; D. Moreira: phy- inferred from large subunit ribosomal DNA sequence data. Algae,
logenetic analysis. 22: 57–67.
Klut, M.E., Bisalputra, T. & Antia, N.J. (1987). Some observations
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