BioSystems, 13 (1980) 65--108 65

@ Elsevier/North-Holland Scientific Publishers Ltd.

ON DINOFLAGELLATE EVOLUTION*

F.J.R. T A Y L O R
Departments o f Oceanography and Botany, The University o f British Columbia, Vancouver, B.C., V 6 T 1W5,
Canada.
(Received October 5th, 1979)
(Revision received April 22nd, 1980)

A broad overview of the diversity o f living dinoflagellates is presented in a hypothetical evolutionary context.
Ultrastructural, and some physiological information is included. Five principal organizational types: prorocen-
troid, dinophysoid, gonyaulacoid, peridinioid and gymnodinoid, are taken to represent lineages, and the
developments within each summarized. Theeal evolution is discussed partly with the aid of a model developed
to determine probable plate homologies in the gonyaulacoids and peridinioids.
Both primitive and highly specialized features are drawn attention to, particularly with regard to the nucleus
and ocelli. The parallelism between the latter and metazoan eyes is extraordinary, considering that the dino-
flagellate organelles are made of subcellular components. The roles o f various types of cysts within the life-
cycle of dinoflagellates are discussed.
The compatibility of the hypothetical events proposed here with the fossil record is briefly considered, and
some indications of the phyletic position o f dinoflagellates are reviewed. The conclusions summarize the
principal developments that appear to have arisen within the group. The relative primitiveness of the desmokonts
is affirmed.
A new combination, Plectodinium miniature (Kofoid and Swezy) comb. nov. is proposed, as well as the recog-
nition of a new order, the Gonyaulacales ord. nov.

'#The answers to these questions are the hidden treasure we seek. But, as I will try to show, it is the
evolutionary view that illuminates the p a t h . "
John Tyler Bonnet,
On Development, 1974.

Introduction

Knowledge of both recent and fossil dino-
flagellates has undergone a considerable
expansion recently. Interest in the living
forms has been excited by a remarkable
variety of features which make the group
both fascinating and complex (reviewed in
part by Loeblich and Loeblich, 1966;
Loeblich III, 1970, 1976; Dodge, 1971 and
Sarjeant, 1974). These include the discovery
of unusual prokaryote-like chromosomes and
idiosyncratic mitoses, the elaborate diffe-
*A contribution from the Society for Evolutionary
Protistology.
mntiation of walls and some internal
organelles, the suitability of some of its
members for observations on bioluminescence
and metabolic periodicity, the significant
contribution to marine and sometimes fresh-
water planktonic primary productivity, the
important associations of dinoflagellate
"zooxanthellae" with many invertebrate and
protistan hosts (including radiolaria, some
foraminifera and all the reef-building corals),
and the peculiar life-cyclesand ultrastructure
of parasitic dinoflagellates (a problem to
tropical fish collectors).
The production of unusual neu~toxins
66

lethal to man, such as "saxitoxin" produced
by species of Protogonyaulax and others by
close relatives (relationships discussed by
Taylor, 1979a), has added to the concern
about "red tides" produced by dinoflagel-
lates, long known to produce marine fauna
mortalities in various parts of the world. The
periodic and extensive fish-kills in the Gulf of
Mexico (Steidinger, 1973), in Japanese bays
used for mariculture (Irie, 1973), and the
production of ciguatoxin in fish (Yasumoto
et al., 1978; Taylor, 1979b) are of particular
economic concern.
Despite this expansion of information, and
the production of a number of valuable
reviews oriented towards palynological inter-
pretations (e.g. Evitt, 1970; Loeblich III,
1970; Wall, 1970, 1971; Harland, 1972;
Sarjeant, 1974) discussions of the evolution
of the group by neontologists have been few.
The present review was produced first for a
meeting in 1974" but the cancellation of the
publication of the proceedings, after a long
delay, necessitated a complete revision on
re-presentation. In the interim two other
publications, those of Loeblich III (1976)
and BShm (1976) dealing with different
aspects of the evolution of the group, have
appeared.
Earlier attempts at the recognition of
trends in the evolution of large portions of
the group by neontologists include those by
Kofoid and his co-workers (e.g. Kofoid and
Swezy, 1921 and Kofoid and Skogsberg,
1928) on the so-called "naked" and
dinophysoid dinoflagellates. Ab~ (1967a)
also ventured some views on the dinophysoids
shortly before his death. A glimpse of Plate 1
may provide one reason why handling the
living forms comprehensively has been
avoided by many.
Here a broad overview of the evolution of
the group has been attempted (with a few
more significant or fascinating examples
highlighted) as it is believed that there is a
need for a revised perspective with which to
view the group, despite the hazards of over-
generalization and superficiality. It is also
hoped that the basic model(s) for the determi-
nation of tabular homologies briefly present-
ed here will provide food for thought.
Although the fossil record is obviously of
direct relevance to the questions at hand,
the information on "soft-part" features
should flesh out the bare bones of resting
cyst morphology to which the record is
largely restricted. It is also likely that some
dinoflagellate types have left no record at all
(see later discussion of the fossil record).

Internal structure
*This is a revision of the paper referred to as "in
press, Micropaleontology Press, Amer. Mus. of The internal structure of dinoflagellates
Natural History", by Taylor (1976a). at the ultrastructural level has been reviewed

Plate 1. A hypothetical "tree", indicating the probable relationships of living dinoflagellates. Placing of a figure
directly on a line is due to lack of space and is not meant to suggest evolution directly through a living form.
Many genera are not shown, especially parasitic forms. 1. Desmokont with single wall unit; 2,3. Prorocentrum;
4,5. Dinophysis; 6. Ornithocercus; 7. Hislioneis; 8. Amphisolenia; 9. Triposolenia; 10. Hypothesized gonyaulacoid
ancestor; 11. Heteraulacus (ffi Goniodoma); 12. Gonyaulax; 13--16. Ceratium; 17. Ceratocorys; 18. Pyrocystis;
19. Pyrophacus; 20. Peridiniopsis; 21. Diplopsalis, Zygabikodinium; 22. Peridinium; 23,24. Protoperidinium;
25. Scrippsiella, Ensiculifera; 26. Palaeophalacroma; 27. Cladopyxis; 28. Podolampas; 29. Glenodiniopsis;
30. Woloszynskia, 31. Gymnodinium; 32. Gloeodinium (in part, n o t Gl. montanum); 33. Dinoclonium; 34.
Symbiodinium (= Zooxanthella?). 35. Dissodinium (some are g o n y a u l a c o i d , others m a y b e near 53); 36.
Tetradinium; 37. Stylodinium; 38. Protoodinium;'39. Oodinium; 40. Chytriodinium; 41,42. Amphidinium,
43. Brachydinium; 44,45. Amphidinium; 46. Kofoidinium; 47. Pomatodinium; 48. Cymbodinium;
49. Craspedotella; 50. Noctiluca; 51. Katodinium; 52. Oxyrrhis; 53. Blastodinium; 54. Hapiozoon;
55. Gyrodinium; 56. Cochlodinium; 57. Polykrikos; 58. Protoerythropsis; 59. Erythropsidinium
(= Erythropsis), 60. Leucopsis; 61. Nematodinium; 62. Plectodinium; 63. Actiniscus (= Gymnaster);
64. Ptychodiscus.
--.%,. ~ ~ ~ L
68
by Dodge (1971, 1973). Features of some of
the more unusual members (parasites,
noctilucoids) will receive a more extensive
treatment in a supplement, prepared by
J. and M. Cachon (in press at this time of
writing), to Chatton's useful but now out-
dated chapter in the first volume of the
Trait~ de Zoologie (1952). Only features of
particular relevance to the present discussion
will be summarized here.
Text Fig. 1 illustrates the basic organiza-
tion of a generalized dinoflagellate. This
TP
Text Fig. 1. A diagrammatic longitudinal section
through a gymnodinoid dinoflagellate. A V : amphies-
real vesicle; Cp: chloroplast; Cr: chromosome; G:
Golgi complex; LF: longitudinal flagellum; M: mito-
chondrion; N: nucleus; PE: pellicular layer; P, PU:
pusule; SS: striated strand; TF: transverse flagellum;
TP: thecal plate; Tr: trichocyst.
shows an essentially eukaryotic organization
common to many other flagellated protists.
However there are several noteworthy
peculiarities by means of which members
of the group may be recognized and which
give suggestions about their evolution.
The commonest arrangement among the
protists is two, anteriorly inserted flagella.
This type is found in only a small percentage
of dinoflagellates, in the "desmokonts",
e.g. Prorocentrum, but this feature may be
used to argue for primitiveness of the
desmokonts relative to other dinoflagellates.
Flagellar dimorphism, found in all dino-
flagellates, is common in protists although it
usually involves an anterior hairy flagellum
and a posteriorly-directed smooth one, e.g.
in many of the chlorophyll c-containing
groups (see Taylor, 1976b, 1978 for details).
The ribbon-like flagellum present in all
dinoflagellates is unusual but not unique to
the group. Some of the pedinelloid chryso-
phytes have a somewhat similar modification
on their single anterior flagellum. The
presence of simple, rather than compound,
flagellar hairs (although sometimes in com-
plex arrangements) on one or both flagella
is unlike chrysophytes and more like
euglenoids. The functional association of
ribbon-like flagellum and surface furrow
found in most dinoflagellates (the "dino-
konts", in which the flagella are inserted
laterally) is distinctive of the group. LeBlond
and Taylor (1976) have discussed the
functional aspects of this arrangement and
the flagellar wave.
In the motile cell ("mastigont") a wall
consisting of multiple cellulose plates may
be absent or developed to varying degrees.
Unlike other cellulose-producing protists
and higher plants this wall (the theca sensu
stricto) is internal, being formed within a
single layer of vesicles, the amphiesmal
vesicles, below the cell membrane. Internal
walls are also formed by other flagellate
groups, e.g. cryptomonads and euglenoids,
but these are of different composition.
In some dinoflagellates other types of

internal skeletal structures may be found.
In Plectodinium miniatum (Kofoid and
Swezy) comb. nov. (see appendix for
details of this proposed change) the nucleus
is surrounded by a curious "basket" and
there are two small mineralized rods at the
anterior end of the cell. The nuclear basket
does not seem to have a counterpart in
other protists although other gymnodinoid
dinoflagellates can have strengthening of
the nuclear envelope (Greuet, 1972a) and
Taylor (1969) has reported the formation
of a layer of platelets around the nucleus
of Gonyaulax pacifica during part of the
life cycle. Some amoebae, such as Amoeba
proteus, have strengthened nuclear envelopes
and there has been speculation that the
radiolarian capsule may be homologous to
the nuclear capsule of dinoflagellates
(Hollande et al., 1962, 1970).
Of greater interest are the paired internal
siliceous skeletons of Actiniscus and ebriids
(considered to be dinoflagellates by
Loeblich III, 1970), the remains of which
contribute to the fossil record. Taylor and
Cattell (1969) described several cells with
dinoflageUate form and an internal skeleton
like an inverted Y as Dicroerisma psilonerei-
ella. The flagella and nucleus were not well
preserved in. the fixed material examined and
it is possible that these cells may either be
of an organism transitional between other
dinoflagellates and Ebria, or a life-cycle
stage of the latter {Paul Hargraves, pers.
comm.).
Delicate organic scales have been found on
the cell surface of Heterocapsa triquetra and
Oxyrrhis marina, and on the flagella of the
latter, by Clarke and Pennick (1972, 1976}
and Pennick and Clarke (1977). They
resemble the body scales of members of the
Haptophyceae (= Prymnesiophyceae) and the
Prasinophyceae (further details in Taylor,
1978). They are probably more common in
dinoflagellates but, like the flagellar hairs,
are usually too difficult to see.
An additional wall layer, the pellicle, may
be present in the mastigont phase of some
69
dinoflagellates. This is a continuous fibrous
layer internal to the amphiesmal vesicles
(Loeblich III, 1970). In this position it m a y
(e.g. Kofoidinium, Cachon and Cachon,
1974) or m a y not be penetrated by tricho-
cysts (Loeblich Ill, 1970), and fiageUar
pores. It is fbrous and can be cellulosic
with or without an acid resistantcomponent
(Loeblich III and Volcani, 1969) although
the flexible continuous wall of Ptychodiscus
(Boalch, 1969) dissolves in sodium hypo-
chlorite (Gaarder, 1954).
It seems most likely that the pelliclediffe-
rentiates into the resistant cell wall, as
suggested by Loeblich III (1970), and forms
the immediate wall of cells which ecdyse
(i.e. shed the theca: cysts formed in this
asexual manner are referred to as ecdysal
or pellicular cysts). It is possible that, if the
pellicular layer of the mastigont is well
developed and resistant, it may become
preserved in sediments and might be con-
fused with cyst remains by observers. The
wall of the fossil genus Dinogymnium,
thought to be the remains of the motile phase
by May (1976) because of the presence .of
pores resembling those of trichocysts and
flagella, but thought to be a cyst wall by
Tappan and Loeblich (1977), strikingly
resembles the general form of modern mem-
bers of Balechina, such as B. coerulea (Dogiel)
Taylor (1976a), but the precise nature of the
resilience of the outer, ridged region of the
latter has not been established yet. If a
pellicular layer is present in the latter, as
this author strongly suspects, it might be
expected to resemble the wall of Dinogymni-
urn. The fossils exhibit apical apertures
through which the contents appear to have
escaped. It is not known if members of
Balechina exit in this manner.
The paracrystalline, fibrous or mucoid
ejectile bodies, referred to as trichocysts or
mucocysts (reviewed by Cachon et al., 1975}
in the peripheral region, closely resemble
those of ciliates (Dragesco and Hollande,
1962} and some flagellates such as the chloro-
monads. Indeed the whole peripheral complex
70
of cell membrane, microtubules, vesicles,
trichocysts and pellicular layer (the complex
being referred to as the amphiesma by
Loeblich III, 1970 and Taylor, 1976a) is
strikingly similar to the cortex of ciliates
(see review by Pitelka, 1969). This resem-
blance has led to the suggestion of a close
relationship between dinoflagellates and
ciliates by Corliss (1975) and Taylor (1976b)
and is consistent with the presence of tubular
mitochondrial cristae in both. Tubular
cristae are also found in many other protist
groups but may have value as an indication
of phyletic position (Taylor, 1978).
In addition to general cell vacuoles there
are unusual paired, vacuole-like structures,
termed pusules, which open by fixed canals,
one at the base of each flagellum. Although
their function has not been fully established
(cf. Cachon et al., 1970; Dodge, 1972;
Taylor, 1973} they have a topological
relationship similar to the contractile vacuoles
or parasomal sacs of ciliates and can be
thought of as invaginations of the cell surface
with extensive, close contact with the cell
vacuole(s) to facilitate exchange.
Chloroplasts may be present or absent.
Dodge (1975) has reviewed their structure.
Typically the thylakoids are grouped in
threes (a very common arrangement),
although there can be considerable variation.
Most distinctive is the presence of three mem-
branes surrounding the chloroplast instead
of the usual two which comprise the chloro-
plast envelope. This peculiarity is shared only
by euglenoids although the pigment com-
position in the two groups is very different,
euglenoids resembling green algae in the
latter, dinoflagellates resembling the Chryso-
phyceae but usually possessing some unique
xanthophylls such as peridinin (pigments
reviewed by Jeffrey et al., 1975).
A most interesting recent discovery was
that the anomalous chloroplasts of
Peridinium balticum and Kryptoperidinium
(Glenodinium) foliaceum are due to associa-
tion with a cryptic endosymbiont in each
case (reviewed by Taylor, 1979a). In the
latter organism an eyespot is present, the
structure of which (mainly the possession of
three surrounding membranes) resembles a
vestigial chloroplast of the dinoflagellate type.
It lies outside the cytoplasm of the endo-
symbiont and can be used to argue that these
dinoflagellates lost their own chloroplasts
after the symbiosis was established (Taylor,
1979).
Whatley et al. (1979), Dodge (1979) and
Sleigh (1979) have discussed possible relation-
ships of the algal flagellates using the
assumption that in many groups chloroplasts
were secondarily acquired by symbiosis.
Taylor (1978) found that it was not necessary
to invoke such a mechanism in order to
establish probable relationships, emphasizing
that flagella, chloroplast and mitochondrial
types seem to have co-evolved in the protists.
The general pattern of relationships within
the dinoflagellates, outlined in this paper,
suggests that photosynthesis has been
repeatedly, independently lost along many
lineages, a similar pattern to the protists as a
whole (Taylor, 1978). Those thought to be
most primitive, the desmokonts, are all
photosynthetic, suggesting that if any sym-
biotic events determined the basic dino-
flagellate chloroplast type, they occurred
early in the evolution of the group. Fucoxan-
thin-containing members seem to possess
recently acquired endosymbionts (see later).
Most dinoflagellates possess highly unusual
nuclear features. The chromosomes remain
relatively condensed during interphase, a
feature which, together with the persistence
of the nucleolus and nuclear envelope
("cryptomitosis": Hollande, 1972), they
share with euglenoids. However unlike the
latter the chromosomes usually appear
fibrillar with transmission electron micro-
scopy, lacking conventional eukaryotic
histones* although small amounts of some
basic protein may be present (see Rizzo and
*An absence of histones has also been reported for
some fungi (Leighton et al., 1971), trypanosomes and
trichomonads (reviewed by Ragan and Chapman,
1978).

Nood~n, 1972, 1974a,b for studies of the
chromatin and associated proteins). The DNA
is not organized into the conventional
"nucleosomes" (reviewed by Bak et al.,
1979) of eukaryotes. Very large amounts
of DNA may be present (for details see
Loeblich III, 1976b) and Rae (1973, 1976)
has found unusually high amounts of sub-
stitution of thymine with 5-hydroxymethyl-
uracil (HOMeU), a modified base known so
far only in some bacteriophage viruses.
Because some of these features (little or no
basic histone, lack of nucleosomes) resemble
the genophores of bacteria the dinoflagellate
nucleus has been considered to be a sign of
the relative primitiveness of the group (e.g.
Loeblich, 1976a,b; Taylor, 1976, 1978}
although the basic eukaryotic organization of
the cell as a whole does not support Dodge's
(1965} proposed for the recognition of a
separate kingdom for them: Mesokaryota,
intermediate between prokaryotes and
eukaryotes.
During mitosis the spindle is exterior to the
nuclear envelope although some microtubules
contact chromosome-associated, dense
granular bodies (kinetochores?) inserted in
the nuclear envelope (Oakley and Dodge,
1974). This arrangement is remarkably similar
to that in hypermastigote flagellates (Ris and
Kubai, 1974; Hollande, 1974; Kubai, 1975)
but there do not seem to be other features
supporting a close affinity between these
groups (Taylor, 1978).
Principal departures from the typical
"dinokaryon" axe found among some of the
parasitic dinoflagellates such as Syndinium,
and also Noctiluca and Oxyrrhis. The lowest
chromosome counts (4--10) are found in
Syndinium and relatives (Syndiniophyceae
Loeblich III, 1976), a common property of
morphologically simple parasites. However
desmokonts also generally have low numbers
(18--69). Within the peridinioids, gonyaula-
colds and gymnodinoids (see next section
for characterization} the number can vary
considerably, the highest numbers being
estimated for Ceratium (284 in C. hirundinel-
71
la). Some of the numbers appear to be double
or treble the lower counts for the lineage,
suggesting that ploidy changes may have
occurred (Shyam and Sarma, 1978).
There has been little study of ultrastructural
changes during encystment, partly due to lack
of control of the process and partly due to
difficulties in obtaining good fixation through
the relatively impenetrable cyst wall. In
photosynthetic species light microscopy
reveals a loss of photosynthetic pigments
with time in the dark and cold, and the
frequent development of a large reddish-
brown, spherical (lipid} body within resting
cysts (unpublished observations and Turpin
et al., 1978). Bibby and Dodge (1972) and
Schnepf and Deichgraber (1972) have
described some of the ultrastructural changes
which occur during (resting?} cyst formation,
such as the formation of numerous lipid
droplets and a decrease in the elaboration
of chromosomal and chloroplast ultra-
structure, other membranous components
also being reduced. These changes are the
type to be expected during dormancy in
many protists which have cysts (see general
view by Corliss and Esser, 1974). It is to be
expected that shrinkage, associated with a
loss of water to slow metabolic rates, should
also o c c u r .
With the exception of the nuclear features,
those internal structures described so far are
not particularly unusual. Some dinoflagel-
lates show great sophistication in their thecal
differentiation (see the section on dino-
physoids, later) but there are also internal
organelles found in some of the hetero-
trophic "naked" dinoflagellates which are
remarkable for their elaborate subcellular
differentiation.
Many of the phagotrophs (including para-
sites} have elaborate cytostomes with pali-
sades or baskets of microtubules, tentacles
and stomopods (e.g. Erythropsidinium,
Greuet, 1969; Kofoidinium, Cachon and
Cachon, 1974), and even in myxotrophs
such as Ceratium a palisade of microtubules
may be found near the presumed ingestion
 72

site (Dodge and Crawford, 1970).

In addition to trichocysts and mucocysts
there are some much more elaborate ejectile
bodies termed toeniocysts and nematocysts
found in Polykrikos and some of the Warno-
wiaceae (Greuet, 1972b; Greuet and Hovasse,
1977). These are produced by the Golgi
apparatus. Some of the nematocysts are
remarkably similar to the bodies with a
similar name in coelenterates (see text
Fig. 3). In this connection one may recall
Garstang's (1962) suggestion, in rhyme, that
the origin of the stinging cells of the coelen-
terates may offer a clue to the origin of the
Metazoa (but, alas, the mitochondrial cristae
are n o t of the same type, cf. Taylor, 1978).
One of the most extraordinarily sophisti-
cated differentiations of grouped structures
for a single function in the protists is that of
Text Fig. 3. Longitudinal section through a nemato-
the ocelli, also found in some members of the cyst of Polykrikos (redrawn from Greuet, 1972b).
Warnowiaceae. Despite their remarkable J: joining piece; O: operculum; S: striker ("pre-
features these organelles have been relatively cateur"); SF: spiral filament (sections); T: toenio-
underrated by most review authors (with the cyst; V: valve.
exception of Grell, 1973, and Piccinni and
O m o d e o , 1975).
T w o ocelli are shown diagramatically in (from Mornin and Francis, 1967). There are
text Fig. 2 A,B and one is also seen in two principal components of ocelli: a
electron microscope section in Plate 3, Fig. 5 hyalosome consisting of a refractile, lami-

Text Fig. 2. Ocelli. Diagrammatic longitudinal sections through the ocellus of Nematodinium (a) and Erythro-
psidinium (b). Ca: canal; Ch: chamber; Fb: fibrillar bands; L: lens; M: mitochondrion; Mz: microtubular zone;
OD: pigment granules; PC: pigment cup; R: retinoid.
 '.. .," •

i- 2 :5 "

.. ,h .

Plate 2. Scanning electron micrographs. Scales indicate microns. Fig. 1. Protogonyaulax (Gonyaulax) tamarensis
with outer amphiesmal membranes missing, revealing the plates (courtesy of L. and A.R. Loeblich III). Fig, 2.
The same species, with amphiesmal membranes intact (author's freeze-dried prep.). Fig. 3. Heteraulacuspolyedri-
cus; apical view. Fig. 4. Protoperidinium schilleri; right side. Fig. 5. Ornithocercus magnificus; left side. Fig. 6.
Ornithocercus quadratus, dividing pair with immature lists.
74

A i

.f'

Plate 3. Scales indicate microns. Fig. 1. Chromo6omes of Scrippsiella (Peridinium) trochoidea (TEM, courtesy of
J. Kalley). Fig. 2. Ceratium vultur; anterior pair of a chain (SEM). Fig. 3. Transverse flagellum in the girdle of
Thecadiniurn inclinatum (SEM). Fig. 4. Perinuclear capsule of Plectodinium, after cell has burst (phase contrast).
Fig. 5. Section through the ocellus of Nematodinium armature (from Mornin and Francis, 1967).
 75

Desmokont Dinokont

A B

Prorocentroid Dinophysoid

Gonyaulacoid Peridinioid Gymnodinoid

E F G
Text Fig. 4. A, B: Basic flagellar arrangements. C--G: Basic thecal types.

nated lens (or "dioptric apparatus": Grell,
1973) and surrounded by mitochondria and
microtubules, with additional microfibrillar
constrictor bands in Erythropsidinium; and a
melanosome, comprising a reddish-brown or
black pigment cup backing a paracrystalline
retinoid (Greuet, 1968, 1970). Between the
hyalosome and the melanosome is a fluid
filled chamber. The ocellus may be situated
laterally, next to the sulcus in Protopsis,
Warnowia, Nematodinium, and Protoery-
thropsis, b u t it protrudes from the anterior
end in Erythropsidinium ( = Erythropsis) and
Leucopsis.
Most o f the structures seem to be expressly
for projecting an image onto the retinoid.
76

Francis (1967) calculated light paths for an
oval lens of approximately similar shape and
refractive index to that of Nematodinium and
concluded that a "zone of focus" should be
formed near the surface of the retinoid. The
pigment cup presumably functions to shield
the retinoid and to absorb light passing
through, thus reducing backscatter. The
organisms are known to be able to point the
lens in different directions in Nematodinium
and even to change the shape in Erythropsidi-
nium, presumably by means of microfibrils.
The shape of the lens in Erythropsidinium
(text Fig. 2B) appears significantly different
from that of Nematodinium. Light paths have
not been calculated for it but it should be
noted that the retinoid in the genus is much
wider (and chevron-shaped} than in Nemato-
dinium and the image collection is over a
potentially wider angle.
The components appear to have evolved
from normal organelles, not requiring any
major structural novelties other than the
highly ordered retinoid. The lens is probably
reserve material accumulated in a laminated
fashion. The chamber forms from a coale-
scence of vesicles. Recently Greuet (1978) has
found that, during reproduction, the retinoid/
pigment cup complex (all within the same
membranous compartment) dedifferentiate
to the point where it can be seen that they
are derived from a chloroplast. The pigment
droplets can be considered homologous to the
plastoglobuli commonly present in chloro-
plasts (and eyespot droplets).
The ocelli exhibit an uncanny parallelism
to the structure of metazoan eyes, with all
the major functional components except for
conduction of signals, constructed entirely
at the subcellular level. More fascinating and
unanswerable with our present conception of
cells is: what can they do with a focussed
image without a nervous system? Generate
ATP? Photochemical products? The species
with these "eyes" are predatory phagotrophs,
Nematodinium also possessing nematocysts
(Momin and Francis, 1967; Greuet, 1970)
with which it can presumably attack cells in
the vicinity of the sulcus, and Erythropsidi-
nium has a complex feeding apparatus. It
seems most reasonable to assume that in
addition to detecting shadow effects due to
potential prey, the focussing function may
serve as a "range finder", nematocysts only

\
Text Fig. 5. Prorocentroid periflagellar platelet patterns (tentative; not to scale) (A) Diagram of the periflagellar
platelets of P. micans. Some platelets equivalent with those in Fig. B are lettered. N o t e additional platelets.
The base of the spine is indicated by dots. Derived from stained light micrographs courtesy of H.A. yon
Stosch. (B) Diagram of a common arrangement observed (plate lettering informal), e.g.P, minimum vat. mariaele-
bourae, P. cassubicum. Modified from Loeblich (1976b) and original observations. (C) The triangular periflagellar
area of P. lima ("marinumform"), with some plate equivalents indicated. " e " may contact " b " underneath " a "
but this could not be determined. Derived from original scanning electron micrographs. The dots indicate a fin-
like crest formed by "a". The relationship of the megacytic growth zone (mz) to the periflagellar area is also
shown.

being fired when the sharpest image is
received on the retinoid.
General organizational types
In the following account, frequent use is
made of a few principal organizational types
in order to avoid formal taxonomic complica-
tions (text Fig. 4 A--G). These include the
flagellar arrangements described earlier:
desmokont and dinokont. By convention the
surface from which the dinokont flagella
arise is referred to as ventral, this also deter-
mining the dorsal, left and right sides by
analogy with animals. The lateral flagella may
arise quite far apart because the longitudinal
flagellum nearly always arises in the sulcus
posterior to both ends of the girdle. The
ribbon-like transverse flagellum always
passes to the cell's left after arising from the
ventral side.
Five basic types can be recognized in the
organization of the outer vesicles and thecal
plates of the motile state of the life-cycle
(text Fig. 4 C--E}. In prorocentroids there are
two large valves and a field of small platelets
surrounding the flagellar pores (designated
here as the periflagellar platelets). In
dinophysoids the theca is still basically
divisible into left and right halves, but a
girdle and sulcus, with c o m p o n e n t plates,
have been superimposed on the pattern, and
there is an additional subdivision of the large
lateral plates.
Gonyaulacoid and peridinioid arrangements
are similar to one another in that the plates
are arranged into five latitudinal series plus
longitudinal, mid-ventral sulcal platelets.
Additional platelets may be formed from,
and lie between these series, and are referred
to as intercalaries, being anterior if located
on the epitheca and posterior if on the
hypotheca. The principal distinction between
gonyaulacoids and peridinioids is here based
on details o f s y m m e t r y (see models later).
Peridinioids show a tendency towards the
77
maintenance o f bilateral s y m m e t r y and the
formation of anterior intercalary plates on
the dorsal side o f the epitheca. Gonyaulacoids
exhibit torsional asymmetrical developments.
Gonyaulacoid intercalary plates, when
present, are usually on the right ventral side
of the epitheca (the so-called "posterior
intercalary plate" is not an additional plate).
In the peridinioids the antapical plates
usually reduce to two due to the reduction
in size of one, whereas the gonyaulacoids
produce an asymmetrical pattern in which
one of the three antapicals becomes pre-
dominant.
In gymnodinoids amphiesmal strength is
achieved by the proliferation of the amphies-
mal vesicles to produce a " h o n e y - c o m b "
effect. Thecal plates, if present, are very
delicate. Plate series are difficult to recognize.
With silver staining, various regions have been
recognized and named (cf. Biecheler, 1952
and Chatton, 1952 for details).
Each of these principal organizational types
can be further subdivided {e.g. ceratioid,
gyrodinoid, noctilucoid...) but these are
thought of essentially as derivatives and will
be introduced later where appropriate.
The ancestral stock: desmokonts?
Most earlier authors (e.g. Bergh, 1881a,b;
Doflein, 1911; Poche, 1913; Kofoid and
Swezy, 1921; Fritsch, 1935) have concluded
that, of recent forms, it is the anteriorly
flagellated desmokonts which are closest to
the ancestral dinoflagellate stock. The reasons
for this are that this type of flagellar insertion
is the most widespread among the flagellates
{most c o m m o n shared character), girdle and
sulcal grooves are absent, and thecal construc-
tion (when present) is relatively simple, con-
sisting of fewer components than in other
thecate types.
How reasonable is this conclusion in the
light of more recent research? Only a few of
the thecate desmokonts, i.e. prorocentroids,
have been examined ultrastructurally. In
78
summing up their studies Dodge and Bibby
(1973) have stressed that the prorocentroids
possess all of the basic structural features of
dinoflagellates: a dinokaryon; amphiesma
with thick thecal plates located in vesicles;
trichocysts; pusules; heterodynamic, structu-
rally dissimilar flagella, and mitochondria and
chloroplasts with structure consistent with
other members of the group. These findings
affirm the closeness of the desmokonts with
other dinoflagellates and their separation into
a separate class, Desmophyceae Smith, does
n o t seem appropriate.
As y e t none of the thin-walled desmokonts
have been examined with electron micro-
scopy. It is not known if genera such as
Haplodinium, Desmomastix, and Desmocapsa
have amphiesmal vesicles, dissimilar flagella,
or dinoflagellate apertenances other than the
dinokaryon recognized with light microscopy.
Several appear to have a cellulose wall con-
sisting of a single unit (Loeblich III, 1970}.
It therefore still seems reasonable to accept
the desmokonts as the closest living forms to
the ancestral stock, this view being based
chiefly on the commonality of anterior
flagellar insertion with other protists, and the
smaller chromosome number. None are
known to produce thick-walled cysts, which
may explain their apparent absence from the
fossil record, but this may merely reflect
insufficient study of their life cycles and such
cysts might not be obviously distinguished
from the acritarchs. Balech (1971) and
Taylor (1976a) have figured gelatinous
sheaths surrounding cells of Prorocentrum.
In P. compressum the valves become dis-
sociated. Balech thought this might be a cyst
of some type. Braarud and Rossavik (1951}
have illustrated the contents of P. micans,
in culture, rounded up within the valves. They
suspected that these round bodies might be
cysts.
Acceptance of the assertion produces the
concept of an ancestral stock which was
anteriorly biflagellated, photosynthetic (no
achloroplastic desmokonts have been
described unless one accepts Protaspis as a
d e s m o k o n t dinoflagellate), possibly athecate
initially but soon forming a rather heavy
theca consisting of two large plates, the
"valves", joined by a zigzag suture, with a
cluster of small periflagellar platelets sur-
rounding one or t w o flagellar pores (text
Fig. 4C).
Little attention has been accorded the
periflagellar platelets in the past and Dodge
(1976} did not make use of them in his
revision of the genus Prorocentrum. Difficulty
in observation led to the view that some of
the bivalvate species may not possess them
(e.g. Loeblich III, 1970; see summary of
earlier treatments in Taylor, 1976a). In all
species of Prorocentrum (which is s y n o n y m u s
with Exuviaella) examined recently, peri-
flagellar platelets are present (see text Figs.
5 A--C}. Although there is variation within
the genus, there are certain features which are
consistent and may be used to recognize
relationships: Loeblich III (1976a) has
illustrated the pattern for P. minimum var.
mariaelebourae and P. cassubicum, with a
brief discussion of the pattern using a number
for each plate. The plate designated as " c "
here may be inclined relative to " a " and thus
appears as two small platelets in Loeblich's
figure of the former.
One valve is more excavated by the peri-
flagellar pore field than the other and this has
traditionally been designated as the right valve
{Biitschli, 1885) in accordance with the
view that the valves are lateral. In some
species, such as Prorocentrum lima (text
Fig. 5C} the degree of excavation is great,
the periflagellar pore field is subtriangular,
and the pores are inclined at a sharp angle to
the plane of the sagittal suture. In those in
which the excavation is more shallow, the
angle subtended by the pores to the sagittal
plane is also shallower (e.g.P. micans, text
Fig. 5A).
Although earlier authors have reported
fewer platelets, the lowest n u m b e r observed
by the present author is 8, with up to 14 in
P. micans. The platelet designated here as
" a " usually gives rise to a ridge or spine.

There is only one platelet between the pores
in the examples given here and this m a y be a
conservative feature.
Loeblich et al. (1979) have reported the
emergence of both flagella from the larger
pore, a situation similar to the dinophysoids.
It is curious that both flagella that can be
seen unequivocally to arise from the larger
pore in their scanning electron micrographs
appear to be of the "whiplash", rather than
the ribbon type. In the one picture in which
a ribbon-like flagellum is clearly present
(their Fig. 7 of P. triestinum) it arises very
close to the spine and some distance from
the whiplash flagellum, similar to the
situation in P. micans (Biecheler, 1952 and
unpublished obs. by the author). There
seem to be several possible interpretations
of this: some prorocentroids do not have
a ribbon-like flagellum; the ribbon-like
flagellum has lost its characteristic form
during preparation; some prorocentroids
have the flagella arising through separate
pores; or the double whiplash flagella arising
from the large pore are associated with a
zygotic condition similar to that found in the
dinokont dinoflagellates. It is clear that
further observations are needed to resolve the
question of flagellar insertion and type
further.
Loeblich III (1976a) suggested that the
valves are equivalent to the epi- and hypo-
thecae of thecate dinokonts, rather than
being lateral equivalents*. He termed the
most excavated valve the epitheca, and the
least excavated the hypotheca, whereas the
reverse seems to be the more probable to this
author if the valves are not lateral equivalents,
in view of the greater excavation o f the hypo-
*Parke and Ballantine (1957) reversed the left and
right valve designations, terming the more excavated
valve the left valve, presumably not intending to
deliberately reverse earlier convention. Loeblich III
(1976a) and Loeblich et al. (1979) have also used the
reverse designation, although they attribute their
orientational terminology to Biecheler (1952). This
author is not able to find such an error in the latter's
work.
79
theca by the sulcus (the region most closely
comparable to the periflagellar area in dino-
konts), this also being consistent with the
pore alignment if one assumes that the larger
pore is equivalent to the flagellar insertion
aperture of gonyaulacoids and the small pore
remains as a vestige (the so-called '~entral
pore": see later section).
A large and a small pore are present on the
ventral side of dinophysoids (see next
section), both flagella arising from the large
pore in the sulcal region, the small "apical
pore" being located in an antero-ventral
position above the sulcus (text Fig. 4D, s e e
also Taylor, 1971). In these organisms the
sulcus is excavated out of the right valve, an
interesting resemblance with prorocentroids
if the valves are taken to be lateral equiva-
lents.
It seems possible that the valves of proro-
centroids could be both the lateral equivalents
(homologues) of the valves of dinophysoids
and the epi- and hypothecal equivalents of
other dinokonts, since prorocentroids are
thought to be the c o m m o n ancestors of both
types.
The dinophysoid radiation
The dinophysoid dinoflagellates, usually
recognized at the level of order, form a well-
defined marine group, all thecate, exhibiting
features which in several respects appear to be
intermediate between the desmokonts (pro-
rocentroids) and other dinokonts. The theca
(text Fig. 4D) is basically divisible into right
and left halves by a sagittal suture (often
with a zigzag edge), interrupted in the ventral
and apical areas where clusters of small
plates surround a large, single flagellar pore
from which both flagella issue (unlike pro-
rocentroids) and a so-called apical pore, not
much bigger than the somatic porulation.
With the exception of the apical platelets the
arrangement and n u m b e r (18 or 19) of the
plates is highly conservative. Cells show lateral
flattening. Thecal expansion prior to division
80
is by a single broad growth zone, the megacy-
tic zone, surrounding the cell, associated with
the sagittal suture, as it is in the prorocen-
troids. In all there is a well developed girdle
and sulcus.
Interrelationships between the genera have
been discussed by several previous authors.
Kofoid and Skogsberg {1928} produced an
enormous, elegantly illustrated monograph in
which the most obvious relationships were
discussed, but a critical evaluation only began
with the careful dissection of the plates by
Tai and Skogsberg {1934). Ab6 (1967a--c)
discussed the evolution of the genera, basing
his primary determinations on the orienta-
tion of the smallest {ventral) hypothecal
plates but, as Balech (1971} has noted, his
work is flawed by m a n y errors of interpreta-
tion and neglect of previous observations.
For m a n y years it was assumed that the
n u m b e r of plates was constant at 17.
Recently detailed plate studies have been
made by Norris and Berner (1971}, resulting
in the discovery of a further small platelet,
and by Balech (in several papers but most
notably in 1971 showing yet another
platelet). Taylor (1971, 1973a) has examined
several species of Ornithocercus with the aid
of scanning electron microscopy, detailing the
consequences of the division process to thecal
development.
The most primitive members are usually
thought to belong to Dinophysis (among
species formerly separated as Phalacroma;
text Fig. 5A,B). Kofoid and Skogsberg {1928}
suggested this because they exhibit the least
degree of morphological specialization. How-
ever it is also possible that the ancestor could
be one of the "microcephalic" genera (text
Fig. 6V), such as Sinophysis or Metadinophy-
sis. There is a general resemblance of form to
the early fossil Nannoceratopis (cf. Gocht,
1972} but the paratabulation of the latter
appears to have some peridinialean as well
as dinophysoid features (K. Piel and W.R.
Evitt, pets. comm. and in press).
Within Dinophysis sensu lato there are
some species in which the girdle and sulcus
are only minimally developed, bearing no
hyaline crests ("lists"), e.g. D. ruudii
(Braarud) Balech. These may represent
primitive forms but too little is known of
their plates to consider this further. Schiller's
{1928} suggestion that his genus Palaeophala-
croma may be ancestral to the dinophysoids
can be discounted as a result of Balech's
(1976b) demonstration of its peridinioid
tablature (similar to Cladopyxis).
Several remarkably gradual morphological
gradients can be discerned in living forms,
strongly suggestive of evolutionary sequences
proceeding from most generalized to most
specialized, even though all are recent
organisms. BShm (1976} has also noted
some of these and provides more examples.
One group, retaining the basic body shape
(text Fig. 6A) for the most part (the excep-
tion being the elongate Oxyphysis; Fig. 6U),
exhibit experimentation with plates, particu-
larly those in the apical plate region. This
group consists of Metaphalacroma, Pseudo-
phalacroma, Oxyphysis, Proheteroschisma
and, with the unusual addition of a left
hypothecal plate, Heteroschisma. The inter-
pretation of the plates in this subgroup was
complicated for a long time by the use of
heavily megacytic specimens for typification.
They appear to represent several short lines
rather than a continuing evolutionary
sequence, with no evident adaptive factors in
operation. Ab~ (1967a) believed that the
elongate genera Amphisolenia and Tripo-
selenia arose from an Oxyphysis stock.
A fascinating and bizarre sequence (text
Fig. 6B--L) is exhibited by the genera
Dinophysis, Ornithocercus, Parahistioneis,
Histioneis and Citharistes (showing such a
gradation that the distinction of some of the
genera is highly arbitrary). The theme of this
sequence seems to be list elaboration, both
girdle and sulcal. Text Fig. 6B--F illustrates
the apparent transformation from Dinophysis
to Ornithocercus, with the great increase in
the size of the left sulcal list (and an
accompanying posteriodorsal extension of the
narrow plate giving rise to it) to produce a
 81

¢ TheDinophysoid

General Morphology

....:...¢5 -o, . _

Text Fig. 6. Dinophysoids (simplified left lateral views, bodies in strong outline, not to same scale). A, B:
Dinophysis (Phalacroma); C--E: Dinophysis; F, G: Ornithocercus; H: Parahistioneis; I--K: Histioneis; L: Citha-
ristes; M: Histiophysis, O--Q: Dinophysis; R,S; Amphisolenia; T: Triposolenia; U: Oxyphysis; V: Sinophysis.

keel-like posterior wing, and extension of
both girdle lists to produce large anterior
collars. Taylor {1971) has pointed o u t that
these modifications seem inimical to con-
ventional dinoflagellate movement. Even if
movement is not completely stopped (sub-
sequent observations on living specimens by
the author show that they do turn slowly),
it should produce an enhanced flow of water
relative to the degree of movement through
the water. Because of a notch in the ventral
edge of the upper girdle list, water from the
anterior should be directed chiefly towards
the sulcus and, as this genus lacks photo-
synthetic pigments, perhaps this modification
serves as a feeding current. Girdle list exten-
sion is taken to its most elaborate extreme
in O. splendidus {text Fig. 5G) in which the
right sulcal list is more delicate and weakly
developed than most members of Ornitho-
cereus.
All the more elaborately winged genera
( Ornithocercus, Parahistioneis, Histioneis
and Citharistes) lack fully developed chloro-
82
plasts. The cytoplasm of many of these has a
distinctly pink or rose hue, the pigment of
which is unknown. Most, if not all, give
shelter to coccoid cyanophytes in the space
enclosed by their upper and lower girdle
lists. The number of coccoid cells, termed
"phaeosomes" by early authors, varies
greatly, but can exceed several hundred. They
are extracellular in Ornithocercus (unpublish-
ed micrographs by Claude Greuet) although
seemingly enclosed by the girdle lists,
adhering loosely to the dinoflagellate surface.
Norris (1967} has cultured two species of
"phaeosomes", naming them Synechocystis
consortia and Synechococcus carcerarius. The
nature of the nutritional, or other interaction,
between the partners, has not been examined
yet.
The most intriguing aspect of the morpho-
logical modification of the most elaborate
members of the Dinophysis-Citharistes series
is the formation of a chamber-like space in
the cavity where the phaeosomes occur, by
the expansion and pouching of the lower
girdle lists and the cell body. The upper girdle
lists have also elongated, providing greater
space in the chamber by becoming very
narrow at the base (the epitheca becoming
minute}, extending upward as a tube until
they flare out distally to roof over, but not
entirely enclose, the chamber {text Fig. 5K,L).
In several members of Histioneis the chamber
also has large lateral pouches formed by the
lower girdle list {text Fig. 5J). In Citharistes
(text Fig. 5L) the enclosure of the cavity has
been achieved by a shift in the orientation of
the lower girdle list relative to the body, with
the upper girdle list effectively moved out of
the chamber altogether.
In these genera there seems to have been
the formation of a special "culture chamber"
for the phaeosomes. If so, the presence of the
phaeosomes has presumably been a potent
determining factor in the development of the
girdle lists of these elaborate genera.
Individuals lacking phaeosomes can be quite
frequently observed, even in Citharistes
(Norris, 1967; Balech, 1971), indicating that
the association is not obligate, thus weakening
this argument, but there does not seem to be
any better idea at present.
Other dinokonts
Most dinoflagellates are recognized here as
derivatives of three primary organizational
~ypes: gonyaulacoid, peridinioid and gymno-
dinoid (the latter including some bizarre
subgroups, such as the noctilucoids, which
might be thought of as derivatives).
The first two types have usually been
placed together in one order (the Peridiniales)
although this paper offers a departure from
that practice. Their thecal tabulation can be
readily subdivided into five latitudinal series:
apical, precingular, cingular, postcingular and
antapical, with rarely more than eight plates
in each, and one cluster of small platelets
surrounding the flagellar apertures (sulcals).
Plates between series have been termed inter-
calaries. However, in gymnodinoids the
amphiesmal vesicles (and any contained
plates} have proliferated, so that the series,
other than girdle and sulcal (often extending
to the apices), have become obliterated. This
distinction is not sharp, and there appears to
be a gradient between peridinioids with
numerous platelets and gymnodinoids
(discussed more fully later).
Wall and Dale (1968a) have recognised the
gonyaulacoid/peridinioid distinction in cyst
lineages. In order to recognise these they used
the plate combination of: 6 precingular,
6 postcingular, 1 posterior intercalary,
1 antapical for gonyaulacoids, and a 7 pre-
cingular, 5 postcingular, no posterior inter-
calary, 2 antapical combination for peridini-
oids, indicating that members had "all or
most" of these characters. This recognition
of two major subdivisions seems to be gaining
acceptance among palynologists.
This author has come to much the same
conclusion, but through a somewhat different
approach. In essence the distinction is made,
not so much on the basis of the number of
 83

A ^

A A
G H I

Id ls
.J la

lp
Ida ,ma I s a
dr~ m m s m

dp mp sp

Text Fig. 7. Basic model tabulation designations (flagellar insertion indicated by A). A: epitheca; B: ventral
surface ; C : hypotheca; D : polar view showing "Y" arrangement ; E : "A" polar arrangement ; F : an alternate basic
equatorial plate arrangement (D--F suggested by W.R. Evitt); G--I: designations for plate subdivisions, using
dexter (right, d), sinister (left, s), antero (a), postero (p) and medio (m) qualifying subscripts. A maximum of
nine subdivisions (Fig. 1 ) can be designated in this fashion.

plates in a n y series, b u t r a t h e r on the and even Ceratium {related to Gonyaulax by

general s y m m e t r y o f organization. T h e basic
m o d e l (Fig. 7) has been previously p r e s e n t e d
briefly {Taylor in Brugerolle and T a y l o r ,
1 9 7 9 ) and has been used t o discuss some
relationships b y T a y l o r ( 1 9 7 9 a ) .
Gonyaulacoids
T h e t a b u l a t i o n o f t h e genera Gambierdiscus,
Coolia, Pyrodinium, Alexandrium, Proto-
gonyaulax and Gonyaulax suggest t h a t t h e y ,
Wall and Evitt, 1 9 7 5 ) , can all be derived f r o m
a h y p o t h e t i c a l p a t t e r n similar to that o f
Heteraulacus (= Goniodoma) by relatively
simple d i s t o r t i o n s o f b o t h the epithecal and
h y p o t h e c a l plates {text Figs. 8B--E, 9B--E,
1 0 F - - H ) , with n o m a j o r additions or subtrac-
tions. If t h e i r plate arrangements are
d e s c r i b e d by the c o n v e n t i o n a l s h o r t - h a n d
n o t a t i o n and " f o r m u l a e " based on the K o f o i d
s y s t e m {1907, 1 9 0 9 ; see Loeblich [II, 1 9 7 0
and Sarjeant, 1 9 7 4 for details) an impression
 84
of major differences is given. Steidinger
(1971) made a start towards this realization
with regard to some of the above genera, but
did not develop the idea very far.
The serious weaknesses of the Kofoid
system, in widespread use for phyletic or
phenetic comparisons, is that plates are
appointed to series and numbered with no
attempt to recognize plate homologies. In des-
criptions this is usually simple to apply (see
Taylor, 1976a, for some problems with
gonyaulacoids), but with no concept as to
what a "basic pattern" for any group might
be reliable homology determinations have been
difficult. Taylor (1979a) has presented a
numbering system for gonyaulacoid genera
as a start towards this goal. In the discussion
which follows the abbreviation TS for
"Taylor System" and KS for "Kofoid
System" {including the customary modifica-
tions introduced after Kofoid developed it)
will be used.
The tabulation of Heteraulacus is particu-
laxly interesting as it is almost radially sym-
metrical, and the epithecal and hypothecal
patterns axe very similar (text Figs. 8B, 9B),
with three polar plates and seven or eight
plates near the girdle on each side. There are
two pores on the epitheca: an apical pore in
its own triangular platelet, and a smaller but
prominent pore on the upper edge on the
plate stippled in text Fig. 8B. The girdle
(cingulax) plates may also be considered as
basically eight (five large and three small).
Two of the small ventral platelets have been
taken to be "sulcal plates" (KS: anterior
sulcal, median sulcal) and a third is arbitrarily
a "transitional" or cingulax plate (e.g.
Graham, 1942; cf. Taylor, 1976a, 1979a).
If the Heteraulacus pattern is simplified by
ignoring apparent plate subdivisions one
arrives at a radially symmetrical model (text
Figs. 7, 8A, 9A, 10E) which can be thought
of as consisting of six longitudinal segments,
three of which axe alternately subdivided at
eacL pole, and all with one further segment
at the equator. Note that the three polar
plates on each side are not subdivisions of the
same longitudinal sectors, but rather alternate
with their counterparts at the opposite pole,
the undivided sectors not reaching the apices
(see text Fig. 7B). Evitt (pers. comm.)
prefers a model in which the equatorial plates
alternate with the pre- and post-equatorial
ones.
Although there is not space here to detail
many modifications from this basic pattern
(including flattening, elongation, torsion,
expansion of one side, plate subdivision and,
very rarely, loss of sutures), a minimal
number of examples are provided here (text
Figs. 8 and 9). Some key plates have been
labelled, using TS designations, to show
apparent homologies. On the epithecae the
pore or notch on the margin of the rhom-
boidal "first apical plate" (TS: ls) (in reality
a modified precingular if this model is close
to reality) provides an additional label for
this suture (TS: A/Is suture), appearing in
Pyrodinium, Alexandrium, Protogonyaulax
and some members of Gonyaulax (where it
may appear more as a marginal notch).
In the hypotheca there appears to be a
progressive asymmetry in pattern from
Heteraulacus to Gonyaulax and Ceratium.
In some (e.g. Protogonyaulax) this has been
due to an increase in size of the right ventral
primary antapical (TS: Z) and a consequent
displacement of the other two {text Fig. 9D).
In Gonyaulax the most dorsal polar plate
(TS: Y) has become enlarged, surrounding
the posterior sulcal (KS: Sp; TS: Z), and
there is a major sutural shift so that the V/VI
suture contacts Y instead of Z* (text Fig.
9D,F).
In addition to distortion (in particular,
torsion accompanied by "left-handed" girdle
displacement) and loss, there has also,
apparently, been plate subdivision (not
*In the type description of Protogonyaulax (Taylor,
1979a) there is an important typographical error in
this regard. In Protogonyaulax the V/VI suture con-
tact~ Z, as in Heteraulacus, and not Y as in Gonyau-
lax. Thus the description should be corrected to read.
"... V/VI contacting Z" (p. 51, line 16) and "...
thecalis polar posterior (Z)" (p. 51, line 23).
 85

~ P

• G~, 1E

r"

)-

EPITHECAE
Text Fig. 8. Hypothetical transformations in epithecal tabulation from radially symmetrical models (flagellar
insertion indicated, "first apical plate" stippled). A: hypothetical gonyaulacoid ancestor ("pre-Heteraulacus");
B: Heteraulacus; C: Alexandrium, Pyrodinium; D: Protogonyaulax; E: Gonyaulax ; F: Ceratium; G: Pyrophacus
(some more subdivided); H: hypothetical peridinioid ancestor; I: Peridiniopsis; J: Dipiopsalopsis; K: Peridinium
palatinum; L: Peridiniopsis, Diplopsalis ; M,N : Protoperidinium, (subg. Archaeperidinium ). O--Q: Protoperidinium
(subg. Protoperidinium ).
86

~ F

HYPOTHECAE

J v

\f
Text Fig. 9. Hypothetical hypothecal transformations from radially symmetrical models (flageilar insertion
indicated, antapical plates stippled). A: hypothetical gonyaulacoid ancestor; B: Heteraulacus; C: Pyrodiniurn;
D: Protogonyaulax; E: Gonyaulax. F: Ceratl"um, G: hypothetical peridinioid ancestor; H: Phthanoperidinium-
like; I: Peridinium, Protoperidinium, Peridiniopsis; J: Diplopsalis, Zygabihodinium.

shown here), exemplified by Pyrophacus,
in which many supernumery plates appear
on both the epi- and hypothecae (Wall and
Dale, 1971).
Ceratium may represent an extreme distor-
tion in this lineage. Marine forms are difficult
to analyze because o f the delicacy of the
midventral plates, but with the aid of fresh-
water species in which the plates on the con-
cave ventral surface are more strongly
developed, a basic gonyaulacoid plan can be
discerned {Wall and Evitt, 1975). In the fresh-
water species the flagella arise from a slot in
the left side of the ventral concavity
 87

Text Fig. 10. Diagrams of representative peridinioid (a--e) and gonyaulacoid (f--h) sulcal plates. Sequence is not
indicative of sequential relationships. Hatching indicates fin position. Dotted areas are probably incompletely
worked out. Number indicates cingular series, a: Peridinium s.s.; b: Scrippsiella sweenyae; c: Scrippsiella subsalsa;
d: Protoperidinium; e: Cachonina ; f: Heteraulacus ; g: Helgolandinium ( Fragilidium and Pyrophacus similar but
cingulars different); h: Protogonyaulax (Gonyaulacysta very similar).

(Bourrelly, 1970; Dodge and Crawford, 1970)
and it seems that one or more plates may be
missing from this region (compare text
Figs. 9C,E). Ceratium is a large genus and
exhibits a remarkable range of modification
of the body (text Figs. l l A - - J illustrates
some of the principal variations). The forms
shown as l l A and l l B are closest to other
gonyaulacoids and have both fresh water and
marine representatives. Other freshwater
forms have remained close to this ( l l C ) , but
in the marine environment there has been a
great diversification. All the latter have the
thinned ventral plates referred to earlier,
apparently to provide a more plastic area
through which both conjugation and phago-
trophy can occur in some species (Von
Stosch, 1964; Norris, 1969). Other modifica-
tions include narrowing and extension of
the whole cell ( l l J ) or its extremities, or the
production of broad leaf-like "paddles" by
the expansion of either the epithecal ( l l G )
or hypothecal horns ( l l H ) . The hypothecal
"fingers" of C. ranipes ( l l I ) are particularly
curious.
These extensions are rigid structures and
have most frequently been assumed to be
adaptions for the increase of surface friction,
reducing the sinking rate when the cells
periodically cease swimming, the effect being
increased by asymmetry of form (Kofoid,
1907). However, BShm {1976), in a review
of the data, could find no support for this
assumption. Another factor which could be
important is an increased efficiency in the
illumination of the chloroplasts in this almost
entirely photosynthetic group. Graham
(1941) noted that species occurring deep in
the euphotic zone (or below it) show the cell
expansion and flattening most markedly
(subgenus Archaeceratium). Taylor (1973)
has discussed these sub-euphotic "shade-
88

Ceratium
Text. Fig. 11. Variability in Ceratium (diagrammatic, not to same scale). Species approximating each type.
A: C. minutum; B: C, candelabrum; C: C. hirundinella; D: C. pulchellum; E: C. lunula; F: C. trichoceros,
G: C. praelongum; H: C. platycorne ; I: C. ranipes; J: C. extensum.

forms" further. The question of resistance to ture) characteristics (reviewed by Sarjeant,

grazing was not considered by BShm but it
may be important and so may nutrient
uptake surface area.
Another feature of unknown significance,
although presumably related to the above,
is autotomy, in which members of some
sections of Ceratium can cut off the distal
parts of the horns, reforming them later.
Resting cysts within t h e gonyaulacoids are
highly varied in gross morphology and, to a
lesser extent, archeopylar (excystment aper-
1974). Most of the "hystrichosphaerid cysts"
are produced by members of this lineage.
Wall and Dale (1968a) have grouped fourteen
cyst lineages (both living and fossil) into this
category including apical, precingular,
cingular and epitractal archeopyles. In
Pyrophacus (= Tuberculodinium) the archeo-
pyle is hypotractal. In Protogonyaulax
catenella and P. tamarensis the zygotic resting
cyst is smooth-walled, usually loosely invested
in mucoid material and excystment is by

apical rupture without the formation of an
operculum. Thus, if found in fossil sediments
it would n o t be assignable with certainty to
the dinoflagellates and would be termed an
"acritarch".
Ecdysis and reproduction within the
accompanying division cyst (= "zoosporan-
gium" in part, of Van Stosch, 1972, 1973},
is c o m m o n in members of the group, e.g.
Pyrophacus, Helgolandinium, these cysts
having a different appearance to the resting
cysts (e.g. those of Gonyaulax reticulata and
G. pacifica: Taylor, 1962, 1969, and
Pyrodinium bahamense, Buchanan, 1968).
Normal, oblique fission also occurs, however.
Ecdysis is most c o m m o n l y by disjunction of
the apical plates in Gonyaulax, but in some it
may be by separation of the epitheca from
the cingulum (Protogonyaulax tamarensis). It
is not known if some of the cysts produced
by ecdysis are fossilizable.
The great majority of the gonyaulacoids
have retained a photosynthetic capacity,
colourless members being rare. Luminescence
is c o m m o n within the lineage, and some of
the members which are close to the basic type
proposed here give rise to potent neurotoxins,
e.g. Pyrodinium, Protogonyaulax (discussed
by Taylor, 1979a). When the modifications
referred to are reasonably compensated for
the conservativeness of the basic sutural
pattern is striking. As with the dinophysoids,
existing forms often provide numerous
examples of apparently gradual transition, so
that morphoclines can be constructed which
strongly suggest evolutionary development,
even though this is a phenetic {current tips o f
the branches) comparison rather than a
phylogenetic (all the branches) reconstruction
and the direction of change can only be
arbitrarily designated. Here it has been
assumed that change has usually been from
simple to complex, watching for possible
reduction when the sequence suggests it.
It must be admitted that the general direction
of change could have been from many to
fewer plates (a possibility raised by the
unfortunately highly incomplete fossil record:
89
see later) but this will be very difficult to deal
with and requires much more information to
resolve. The n u m b e r of convincing examples
of apparent suture loss in living dinoflagellates
are very few {e.g. Ceratocorys in the gonyau-
lacoids and several in the peridinioids: see
below}.
Peridinioids
Peridinium-like patterns can also be
reduced to one similar to the "pre-Heteraula-
cus" model, i.e. one with three polar, six pre-
and post-equatorial plates and a similar (but
not identical) sulcal plate arrangement. The
girdle plate number has been considerably
modified in some, e.g. reduced to three out-
side the sulcal region in Protoperidinium.
Despite this similarity, there is an interesting
difference when the pattern is reduced to a
hypothetically radially symmetrical model:
the plate which seems to have formed the
first apical plate (KS: 1'} does not obviously
reduce to the subdivision of a pre-equatorial
plate, but instead seems to obviously repre-
sent a whole pre-equatorial plate. The
orientation of the polar plates relative to
the flagellar insertion is also different.
Instead of the " Y A " polar plate orientation
of gonyaulacoids, it seems to be an " A Y "
orientation (see text Figs. 6--9). It is
possible that the plates conventionally
referred to as first apical plates are not
homologues in gonyaulacoids and peridinioids
and it is most probable that they are deriva-
tives of preequatorial ("precingular", KS)
rather than polar plates as their name implies.
What is not clear is how the plates of
gonyaulacoids and peridinioids relate to each
other. If this could be established (and the
intercalaries confidently assigned to ancestral
plates) the alternative plate homology desig-
nations of Taylor (1979a) could be given to
peridinioids as well as gonyaulacoids. How-
ever, no satisfactory evidence has come to the
author's attention which can resolve this
dilemma at present. It was hoped that a
careful consideration of the position of the
90
fission line, or plate overlap patterns would
be of assistance but it has revealed that both
are very similar, with no obvious displacement
of the flagellar insertion from one sector to
another. The fission line runs through the
sulcus in both, and in both the midventral
plates (including the KS first apical) are
overlapped by all adjacent plates (cf. Durr and
Netzel, 1974, and Gocht and Netzel, 1974).
The principal possibilities seem to be as
follows:
(1) The first apical plates correspond to
adjacent pre-equatorial sectors of the basic
symmetrical model, the plate overlap being a
later parallel development in both.
(2) The first apical plates are from the same
longitudinal sector but on opposite "hemis-
pheres", the cell directional orientation being
reversed in the two types (a "flip-flop"
model).
(3) The first apical plates are homologous,
but distortional events have produced an
apparent change in basic s y m m e t r y .
The second alternative, while solving the
problems of similarity in overlap pattern and
fission line, seems to be the most radical (and
least probable?) If the transverse flagellum
beat to the left in peridinioids instead of to
the right it might support this alternative, but
in fact the transverse flagellum of all dino-
flagellates with a well-developed girdle beats
to the cell's left after it leaves its point of
origin.
It is striking that the similarities between
gonyaulacoids and peridinioids extends to the
small platelets of the sulcal region. In both
there is an anterior sulcal plate (which may
cleave into two in many peridinoids, e.g.
Scrippsiella, Protoperidinium, one moiety
then being referred to as a cingular or transi-
tional plate: text Fig. 10B), two elongate
larger platelets in the midregion, one or two
very small platelets where the flagella emerge,
and one large posterior sulcal which seems to
be derived from a posterior polar plate. How-
ever the latter, designated as " Z " by Taylor
(1979a) in gonyaulacoids, bears a different
symmetrical relationship to the other two
polar plates in peridinioids and is therefore
probably not homologous to Z.
These similarities, taken together, suggest
that the s y m m e t r y differences between the
two lineages may be due to secondary dis-
tortive influences (option 3 above) rather
than a separate development from an ancestor
still near the hypothetical radially-symmetri-
cal pattern. In text Fig. 8 both possibilities
are shown, a species such as the fresh-water
Peridinium palatinum (see Bourrelly, 1970
and the epithecal pattern in text Fig. 8K)
offering an example of a peridinioid which
could have arisen as a distortion form from
the gonyaulacoid type.
With the information available further
speculation seems futile at the m o m e n t
although the thecal relationships between
these two major dinoflagellate lineages is an
important question for which at least a
reasonable hypothesis must be forthcoming
to permit the use of a unified model and
numbering system of plate homologies.
Among the peridinioids there are members
with no apical pore (Dinosphaera, some fresh-
water Peridinium attributed by some to
Cleistoperidinium, Glenodiniopsis), some in
which the pore has formed at the natural
apex of the first apical plate (8 I,J, e.g. some
Peridiniopsis, Diplopsalis, Zygabikodinium,
Entzia), and m a n y in which it has formed at
the junction of the three primary polar
plates (8L--Q including most of the marine
peridinia attributed by Balech, 1974, to
Protoperidinium, as well as Scrippsiella and
Ensiculifera). In the latter cases, an additional,
small, elongate platelet has formed between
the pore and the apex of the first apical.
Balech (1974) has termed this small addition
the " x " plate. The presence of this platelet
is consistent with the model although the
designation of Balech should not be con-
fused with the antapical X plate of Taylor
(1979a).
The alternate positions for the apical pore
(at the primary apex or ventrally displaced)
illustrates another weakness in the current
system o f plate terminology. In text Fig. 8 I

the letter a marks a plate that must be called
an intercalary plate by present convention
since it does not contact the apex. However
it is obviously the homologue of one (mid-
dorsal) o f the apicals in 8L, and the a plate
in 8P is not homologous to the whole plate
in 8L. Note also that all those in question are
hexagonal, illustrating an unavoidable weak-
ness in attempting to determine the plates
represented by archeopyles of particular
shapes in cysts in which reflected tablature
is absent (e.g. Evitt, 1967). Balech (1967)
has also drawn attention to this.
The production of one to four or more
"anterior intercalaries" is a major theme of
this lineage although intercalary plates are
also found occasionally in gonyaulacoids.
Although it might seem simpler a priori to
visualize a symmetrical subdivision of the
mid<torsal apical plate (or precingulars
adjacent to it). present-day representatives
of Protoperidinium, subgenus Archaeperidi-
nium, with two anterior intercalaries (e.g.
P. minutum, P. excentricum) suggest that this
may have occurred asymmetrically, with sub-
divisions occurring chiefly in the upper left
quadrant of the cell (text Fig. 8M), the plates
subsequently shifting to form a more bilater-
ally symmetrical arrangement (8N). An
asymmmetrical subdivision of plates in the
same region is also seen in Peridiniopsis
asymmetrica and related ovoid genera (Plate 1,
Fig. 21).
In the peridinioid lineage there are some of
the most convincing examples of what is
apparently a relatively rare occurrence in
dinoflagellates: the loss of sutures. In marine
Diplopsalis (= Dissodium ) and Zygab ikodinium
the mid-antapical suture has disappeared (9J),
all other sutures and plates being in a similar
position to those in other genera (e.g. Peri-
diniopsis) and almost identical in other
respects (text Fig. 9 I). In the apparent
relatives of Peridinium there may have been
a progressive loss of sutures separating the
girdle plates, the least n u m b e r (3 or 4)
occurring in the marine peridinia transferred
to Protoperidinium by Balech (1974). There
91
is no sign o f plates being displaced, the sulcal
plates being much the same as in those with
five or six girdle plates {text Fig. 10). This
reduction in plate number seems to have
occurred in parallel with a loss in photosyn-
thesis, nearly all members of Protoperidinium
being non-photosynthetic now that several
photosynthetic species have been transferred
to Scrippsiella, e.g.S, trochoidea. In gonyau-
lacoids an example of apparent loss o f suture
is in Ceratocorys where a suture on the dorsal
tight side of the sulcus is apparently missing.
Whereas left-handed girdle displacement is
the most c o m m o n condition throughout the
dinokonts, in some peridinioid lineages
(particularly those with a para/hexa combina-
tion) a slight tight-handed displacement is
c o m m o n . BShm (1976) has analyzed trends
in girdle displacement in relation to tabula-
tion type ("ortho", "mete", "pare") in
Protoperidinium (his "marine forms") and
Peridinium (his "fresh water forms"), finding
some strong correlations.
Horns, particularly antapical extensions,
are well developed in the sections Oceanica
and Divergeatia of Protoperidinium (of which
P. elegans is an extreme example). In
Cladopyxis (Plate 1, Fig. 27) five to ten long,
distally branched processes have been pro-
duced from plates on the dorsal side of the
epitheca and ventral side of the hypotheca,
the processes thus lying in a plane oblique
to the girdle. The tabulation is essentially
similar to that of Palaeophalacroma (Plate 1,
Fig. 26) and Sinodinium (Balech, 1964, 1967)
and the three probably constitute a sublineage
recognizable as a family, with Cladopyxis as
its extreme living member. Despite its rather
cyst-like appearance (reminiscent of some
hystrichosphaerids, but not in actual arrange-
ment of processes) there is no doubt that
these are perfectly normal vegetative cells
(Balech, 1964), the plates being readily
separable from each other and with a normal
thecal appearance, including pores, visible by
scanning electron microscopy (Taylor, 1976a).
Another oddity is the loss of a defined
girdle or even girdle plates in the Podolampa-
92
daceae (genera Blepharocysta, Lissodinium
and Podolampas, Plate 1, Fig. 28). The
remaining plates are quite consistent with the
other plate series normal for the peridinioid
line, leaving little doubt as to the plates which
are missing. Members of the Cretaceous cyst
genus Broomea bear a superficial resemblance
to elongate members of Podolampas, such as
P. palmipes and P. spinifera (cf. Balech, 1963,
1967, and Ab6, 1966) and cingular markings
are "weakly indicated or not at all" (Sarjeant,
1974), suggesting that this anomaly may have
begun some time ago (Mesozoic?). However,
the archeopyle appears to be intercalary in
Broomea, and modern Podolampas do not
have intercalary plates.
Most peridinioid cysts show little paratabu-
lation, a major exception being Palaeoperi-
dinium. They have archeopyles which nearly
always involve anterior intercalary plates
(Wall and Dale, 1968; Lentin and Williams,
1975). The cavate or bicavate condition is
found chiefly within this lineage (Psaligonyau-
lax being an exception). Wall et al. (1970)
have demonstrated that some of the marine
peridinia, suggested earlier to have diverged
before the reduction in girdle plate n u m b e r
(Scrippsiella, Ensiculifera) produce primarily
calcified, spinose resting cysts resembling the
fossil calcionellids. S. trochoidea also makes
the point once again, that several "cysts" can
occur in the same life cycle, for it has ecdysal
vegetative reproduction, the emergent ecdysal
cyst having a smooth, flexible wall, lacking
girdle signs. The cyst o f Peridinium faeroense
(transferred to Scrippsiella by some authors)
would be referred to as an "acritarch"
( u n k n o w n affinity) if it was found by palyno-
logists (Dale, 1978).
Gymnodinoids
The third primary dinokont lineage
recognized here is the gymnodinoids. These
are dinoflagellates in which thecal develop-
ment is de-emphasized and peripheral strength
obtains from a proliferation of the amphies-
mal vesicles in a h o n e y c o m b fashion (as in
ciliates) with or without additional pellicular
support. It is from this group that the greatest
diversification of form, life-cycle, and internal
complexity may have arisen within the dino-
flagellates, only a small part of which can be
illustrated in Plate 1.
The gymnodinoids may have arisen from
peridinioids, or gonyaulacoids (or along
several lines from both). A present-day
example of such a taxon which could be
referred to either peridinioid or gymnodinoid
lineages is Woloszynskia (Plate 1, Fig. 30; c.f.
Crawford et al., 1971; Dodge, 1967; and
Crawford and Dodge, 1971; and compare
with Gymnodinium fuscum, Dodge and
Crawford, 1969). Von Stosch (1973) has
described the thecal pattern and variability of
W. apiculata, as well as life cycle details of
both it and Gymnodinium pseudopalustre.
It is likely that the reduction of the thecal
elements could have occurred along several
lines, and not simple one as implied by the
" t r e e " in Plate 1. However it is very difficult
to obtain convincing evidence of this. Perhaps
one of the best examples of where this may
have occurred is Gymnodinium catenatum.
This gymnodinoid forms chains (as the name
imples). When it was first observed under
routine analytical conditions it was confused
with Protogonyaulax (Gonyaulax) catenella
(Graham, 1943). The size and shape of the
cells are very similar to P. catenella. Although
not evident from the original description the
girdle displacement (left-handed, of one
girdle width) seen in material from Mazatlan
provided by courtesy of G. Morey-Gaines, is
the same and there is a marked furrow which
demarcates an apical area of similar shape to
a gonyaulacoid apical closing plate. Further-
more the gymnodinoid species generates a
nerve poison, as does the thecate taxon.
This circumstantial evidence strongly sug-
gests that G. catenatum and P. catenella
m a y represent closely related forms in which
the thecal plates have been reduced (or
elaborated) in response to a mutational event.
It will be interesting to learn of the com-
parative biochemistry of the toxins produced
by both.

In the "typical" gymnodinoids the girdle
is median in position {Plate 1, Fig. 31), but it
has apparently shifted towards the anterior
in Amphidinium {Figs. 41, 42, 44, 45) and
posterior in Katodinium and Oxyrrhis {Figs.
51, 52). Amphidinium could also have arisen
separately from the dinophysoids (in which
the girdle is premedian) but there is no
evidence for or against this idea. Some of
the presumed Amphidinium sub-lineage have
produced flexible walls and unusual, arm-like
processes such as Brachydinium {Figs. 4 3 ) -
at first thought to be a non-motile state when
seen preserved {Taylor, 1963) but since found
to not only have flagella, but also to wave its
"arms" back and forth {J. and M. Cachon,
pers. comm.).
In some modifications from the basic
gymnoidinoid the motile phase is not the
principal life cycle stage. For example in
Dissodinium {Plate 1, Fig. 35), members of
the Phytodiniaceae such as Cystodinium,
Tetradinium (Fig. 36) and Stylodinium
(Fig. 37), zooxanthellae such as Symbiodi-
nium (Fig. 34) and palmelloid (Fig. 32) and
filamentous {Fig. 33) forms, the motile phase
is ephemeral and a continuous-walled {"cyst")
stage has become the principal "vegetative"
state. A parallel example can be found in the
gonyaulacoid line where the principal phase
of Pyrocystis is apparently a vegetative cyst
derived from Protogonyaulax {Taylor, 1972,
1979a; Swift and Wall, 1972). A variant on
this is found in Dinamoebidium, where the
motile stage becomes amoeboid before
forming a division cyst (Pascher, 1916).
Amoeboid stages have also been reported for
species of Stylodinium and Cystodinedria
parasitic on algae (Pfiester and Popovsky,
1979).
An ever-inCreasing number of parasitic
dindflagellates are being subjected to electron
microscopy (e.g. Haplozoon, by Siebert and
West, 1974), often with surprising results. It is
here that one finds the greatest diversity in
nuclear features, often differing from one
stage of the life-cycle to the next.
Although probably most, if not all,
93
parasitic forms are gymnodinoid derivatives,
it appears that parasitism m a y have arisen in
several different lines, some of which are
shown in Plate 1. For example at least two
species of Dissodinium, D. pseudocalani and
D. pseudolunula, have been described as
parasitic on copepod eggs (Elbr~ichter and
Drebes, 1978) although others having lunate
cysts resembling them (referred variously to
Pyrocystis: Elbr~ichter and Drebes, loc. cit.,
or Dissodinium, Taylor, 1976a) do not
appear to be.
Blastodinium, a gut parasite of copepods,
stillretains its chlorophyll despite its habitat.
The parasitic members of Dissodinium have
been suggested to belong to the same order,
Blastodiniales, as the former because of the
common property of reproduction by
"palintomy", a c o m m o n form of asexual
reproduction in parasitic flagellates, i.e. by
"binary fission repeated over and over again,
without the intermediate stage of nutrition
and growth, leading to the formation of
complete identical products of reproduction"
(Elbr~ichter and Drebes, 1978, p. 355). A
modification of this, "palisporogenesis"
(Chatton, 1952) differs in that the initial
unequal division gives rise to a larger tropho-
cyte which continues to feed from the host,
and a gonocyte which undergoes repeated
division to produce sporocytes and spores,
a new gonocyte arising from the trophocyte
with each unequal division of the latter. This
form of reproduction is found in Blastodinium
and closely related members of the Apodini-
aceae and is the main criterion for recognizing
members of the family.
One of the least differentiated parasitic
forms is Protoodinium. The feeding stage
{"trophont" or "trophocyte") is a typical
small gymnodinoid cell with delicate thecal
platelets, girdle and sulcal grooves, flagella,
trichocysts (usually missing in parasitic forms)
and developed chloroplasts {Plate 1, Fig. 38).
However, it produces a tentacle-like
"peduncle" from the lower end of the sulcus
by means of which it penetrates its host,
remains attached, and draws in nourishment.
94
The peduncle is rather reminiscent in position
and function to the s t o m o p o d of Erythro-
psidinium. More altered feeding stages can be
seen in the ectoparasites Oodinium and
Chytriodinium (Blastodiniales) which also use
stalk-like peduncles to penetrate their hosts
and have lost their photosynthetic ability.
Another distinct assemblage among the
bewildering diversity of parasitic dinoflagel-
lates is the order Syndiniales, united by a
c o m m o n form of mitosis, the presence of
centrioles, and expanded interphasic chromo-
somes. Hollande (1975} has discussed mem-
bers of this group, recently named by
Loeblich (1976a) as a replacement for the
same Coccidiniales. It is this group that has
been thought to be closely related to hyper-
mastigld flagellates on the basis of their
nuclear features (Ris and Kubai, 1974).
Some parasitic dinoflagellates are so modi-
fied that they may strain credulity when seen
attributed to dinoflagellates. Perhaps
Haplozoon exemplifies these (Plate 1, Fig. 54)
and must serve as a final example of the
parasitic forms. H. axiothellae, a gut parasite
of a marine annelid, has been studied by
Siebert (1973} and Siebert and West (1974}.
Its multicellular form has three different cell
types, the anterior-most "trophocyte"
bearing a suction apparatus with numerous
small spines and a large stylet by which it
penetrates a host epithelial cell, several "gono-
c y t e s " behind it undergoing division, and
quadrinucleate sporocytes at the other end.
Surprisingly, the cells of this multicellular
stage have typical amphiesmal vesicles with
thin plates. In other words, each of these
attached cells appear to be equivalent to a
motile cell in structure, except for the lack of
flagella, and pusules, chloroplasts, and tricho-
cysts are also absent.
Ultrastructural information, particularly
that on mitotic mechanisms, may permit the
clearer recognition of parasitic affinities in the
near future.
One major development within the gymno-
dinoids is that in which the mastigont has
undergone left-handed girdle displacement
(the ends meeting the sulcus not lying in the
same plane, the left-hand end being more
anterior than the right), often accompanied
by torsion so that the sulcus is twisted to a
greater or lesser degree. It is also within this
line that nuclear capsules are most c o m m o n l y
found. The simplest form is seen in
Gyrodinium (Plate 1, Fig. 55), the most
extreme torsion occurring in Cochlodinium
(Fig. 56). In C. angustum the girdle takes
four full turns around the b o d y , the sulcus
also spiralling around with it (see Kofoid and
Swezy, 1921, still the most extensive discus-
sion of general form in " n a k e d " taxa).
Another curious development is in Polykri-
kos where displacement is slight, and torsion
negligible, but it appears to consist o~
multiple individuals fused into one. The
number of individuals involved is suggested
by the external morphology since there are
multiple girdles and paired flagella (adjacent
sulci are confluent}. Within the genus the
number of individuals in a chain varies but
often there are fewer nuclei than individuals
(Chatton, 1952}. Here Clifford Dobell's term
"acellular" seems most apt to refer to
Polykrikos mastigonts. Most are non-photo-
synthetic (containing nematocysts) b u t a
few are pigmented, including P. lebourae
which seems to exist in photosynthetic and
non-photosynthetic forms which are other-
wise identical.
The most elaborate products of the gyrodi-
noid line are the ocelloid genera (Plate 1,
Fig. 58--61) referred to earlier in the section
on internal structure. Not only do they
possess ocelli and, in Nematodinium, nemato-
cyst-like ejectile organelles, but some (e.g.
Erythropsodinium) also have a remarkable
posterior extension termed a " p i s t o n "
(Greuet, 1969}, capable of being whipped out
very rapidly to many times its resting length.
It is probably an elaborate homologne of the
simpler tentacle of Protoerythropsis (Fig. 58)
and, possibly, the peduncle o f some ectopara-
sitic genera. These predators also have an
elaborate "stomopharyngean c o m p l e x " for
prey ingestion.

A gyrodinoid side-branch probably gave
rise to Plectodinium (Fig. 62), whose external
morphology is very similar to members of
Gyrodinium and simple Cochlodinium
species. However, the nuclear capsule is an
elaborate basket (Plate 3, Fig. 4) and there are
two internal mineralized spines located near
the apex (not one as sometimes reported). A
comparison of this organization with that of
Actiniscus (= Gymnaster) (Fig. 63)reveals
considerable similarity, the principal distinc-
tion being the elaborate stellate form of the
paired internal siliceous elements in the latter
(found fossilized in sediments dating back to
the Cretaceous}. In Amphilothus, Monaster
and Achradina the internal skeleton is basket-
like and no perinuclear capsule has been
reported for them. Consequently they are not
evidently close to Actiniscus and thus may
constitute a separate gymnodinoid line.
The final examples to be considered here
are the bizarre, mostly warm temperate to
tropical marine relatives of Noctiluca, usually
over-looked by all but a few French plank-
tologists studying the Mediterranean. Three
families are recognized (Cachon and Cachon,
1969) which can be considered sublineages
here. In two, the noctilucids (Fig. 50) and
kofoidinids (Figs. 46, 47) the mature masti-
gonts are much swollen by vacuoles (not
pusules), the former reaching or exceeding
2 mm. Noctiluca has only one flagellum,
and has an elongate tentacle containing
microfibrillar bundles which permit it to be
waved around. Some of the kofoidinids also
have a noctiluca-like stage (e.g. Spatulodinium)
but they are strongly flattened laterally and
both flagella are present. In Kofoidinium and
Pomatodinium extracellular "shells" are held
by special projections of the cell, and may
be rotated! (J. Cachon, pers. comm.). In the
third sub-lineage, the leptodiscids (Figs. 48,
49), the body has been flattened apico-
antapically and the most elaborate forms
(e.g. Craspedotella) have skirt-like extensions
which they can contract in beats resembling
the movements of medusae.
Most of this final group pass through an
95
early stage (the sporocyte) which resembles
members of Amphidinium (Cachon and
Cachon, 1967}, and this seems to be the
only clue as to their origin.
Encystment in the gymnodinoids is com-
monly for vegetative reproduction, additional
to regular binary fission. Klebs (1912) and
Kofoid and Swezy (1921) have described
some of these division cysts, illustrated by
many authors including Pouchet {1883) and
SchStt (1896} but often ignored in discus-
sions of dinoflagellate life cycles. Unlike the
ecdysal division cysts of peridinioids and
gonyaulacoids, gymnodinoid division cysts
may be exogenously produced by the libera-
tion of material. It is unlikely that they
would fossilize. Klebs (1912) distinguished
between "Schleimcysten" and "Hautcysten",
indicating that sometimes the latter may be
formed subsequent to the initial formation of
the more ephemeral mucilagenous layer. An
ephemeral envelope may also form prior to
the formation of resting cysts. Von Stosch
(1973} has referred to a "preliminary wall"
formed in Gymnodinium pseudopalustre
prior to the development of the spinose,
hypnozygotic resting cyst. Resting cysts
have only been rarely seen in gymnodinoid
forms (e.g. Polykrikos) and have variable
forms (cf. Wall and Dale, 1968, Plate 4,
Figs. 27--30).
Biochemical features
Although there has been only one review
specifically directed at dinoflagellates in more
than a decade (the dated but still useful paper
by Loeblich III, 1967) the group has been
included in several comparative texts such as
Stewart (1974) and Ragan and Chapman
(1978}. The latter, being focused on the
phylogenetic interpretation of biochemical
data, is a mine of information and would
render a more cramped abstraction here
redundant and inadequate. Consequently
only a few salient features will be noted and
the reader should consult the above for a
proper perspective on the data.
96
The chloroplast pigments of dinoflagellates
have been described and evaluated by Jeffrey
et al. (1975). In addition to chlorophyll a
dinoflagellates possess chlorophyll c, like
m a n y algae (the " C h r o m o p h y t e Series" of
Taylor, 1978, derived from Christensen's
" C h r o m o p h y t a " , 1962}. However most of
the "chlorophyll a + c algae" possess two
forms of chlorophyll c: c~ and c2. The only
groups which possess only one form (c2 only)
are the cryptomonads and the dinoflagellates.
Taylor (1978) considered this supportive of
the view that they are primitive. Their
carotenoid accessory, pigments, including
acetylenic xanthophylls, also resemble those
of the c h r o m o p h y t e series although a unique
pigment, peridinin, is the principal carotenoid
in most, usually in combination with diadino-
xanthin, dinoxanthin, /~-carQtene and an
unidentified pink xanthophyll. The peridinin
is tightly bound to chlorophyll a and protein
in a unique functional complex (Haxo et al.,
1976). Phycobilins have not been reported for
dinoflagellates although some, such as
Balechina coerulea, possess blue granules of
u n k n o w n composition, possibly similar to
those in some ciliates such as Stentor.
Two of the five species reported by various
authors to contain fucoxanthin, absent in the
majority of dinoflagellates but a dominant
xanthophyll in the Chromophyte Series, have
been shown to harbor symbionts (see earlier
in this text) whose chloroplasts are the cause
of the anomaly. These also possess both forms
of chlorophyll c and do not have the triple-
membrane enclosure of their chloroplasts. It
will be interesting to see if a close examina-
tion of the others with anomalous pigments
(several Gymnodinium spp., their Exuviaella
sp. was not a dinoflagellate) will also reveal
the presence of symbionts. The pattern of
distribution of photosynthesis in the group
as a whole (Plate 1) suggests that photosyn-
thesis has been lost along many lines, rather
than independently gamed.
The formation of starch as a storage pro-
duct is unlike the Chromophytes, although
it is another feature shared with crypto-
monads. Starch is a principal storage
product of the chlorophyll a + b containing
Chlorophyte Series (except euglenoids).
The sterol composition of dinoflagellates
has only been recently examined. The
presence of a unique a-methylsterol, dino-
sterol, in addition to cholesterol, has been
reported (Shimizu et al., 1976). This sterol
resembles another unusual sterol found in
zooxanthella-containing gorgonians, "gorgo-
sterol", and "acanthasterol" isolated from the
coral-eating starfish Acanthaster and may
serve as an indicator of the presence of the
group. Its presence in Black Sea sediments has
been used to suggest dinoflagellate dominance
(Boon et al., 1979).
The lack of conventional histones has been
noted earlier in connection with the dino-
karyon. The nuclei of a few, principally in the
Syndiniophyceae, do stain with Fast Green as
if histones were present. This group of
parasites are also different from other dino-
flagellates in the dispersion of their chromo-
somes during interphase and the possession of
centrioles. However the form o f their motile
cells and the presence of amphiesmal vesicles
and typical dinoflagellate trichocysts during
their life-cycle clearly indicate their dino-
flagellate affinity. Loeblich III (1976a,b) and
Ragan and Chapman (1978) have reviewed
data on the nucleic acids of the group.
Nutritionally the photosynthetic dino-
flagellates show similar requirements to
diatoms. However many diatoms can manu-
facture vitamin B-12 whereas all photosyn-
thetic dinoflagellates require it (cf. Provasoli
and Carlucci, 1974), a characteristic which
probably has considerable ecological signifi-
cance as well as being of evolutionary note.
None of the photosynthetic members can
survive on acetate or sugar in the dark.
Luminescence, of undecided function, is
c o m m o n in the gonyaulacoids (Taylor,
1979a) such as Pyrodinium, Protogonyaulax,
Ceratium and Pyrocystis. However it is also
known from some species of Protoperidinium
and the presumed gymnodinoid derivative,
Noctiluca, is renowned for it. The reaction

of the luciferin with the luciferase is regulated
by changes in cell membrane permeability
(Sweeney, 1974) and the binding of the
enzyme to unique guanine crystals, "scintil-
lons" (Hamman and Seliger, 1972). However
the latter can also be present in non-luminous
dinoflagellates (Gold and Pokorny, 1973).
The toxins of dinoflagellates have attracted
considerable interest (see numerous papers in
the volume edited by Taylor and Seliger,
1979) but their synthesis and function are
still little understood. The best known,
"saxitoxin", has also been reported to be pro-
duced by a blue-green alga, Aphanizomenon,
which might be thought to suggest some
affinity. However it is also similar, if not
identical to poisons produced by salamanders
and one species of Australian octopus. It is
noteworthy, however, that most of the
nerve-poison producing dinoflagellates appear
to be "lower" gonyaulacoids (Taylor, 1979a),
one species of Prorocentrum and Gymno-
dinium catenatum (see section on gymno-
dinoids) being notable exception. Other types
of toxin occur within the genera Gymnodi-
nium and Amphidinium.
The fossil record
The dinoflagellate fossil record is full of
information and there are probably more
taxonomists studying fossil dinoflagellates
than living ones. Sarjeant (1974) has provided
one of several general reviews of the nature
of the record. The intention of the present
paper has been to augment this direct phylo-
genetic data with an interpretation of the
"soft part" information which is used con-
siderably by protistologists to discuss
possible relationships among living organisms
and most of which is unlikely to ever be
available to those studying fossil remains. The
biological significance of many fossil features
has been illuminated by the studies on living
dinoflagellates by Evitt, Wall, Dale and others,
focused on this aspect (earlier work reviewed
by Wall, 1971).
97
Unfortunately, if one wishes to determine
the compatability of relationships and
sequences proposed here with the fossil
record a number of relations severely limit
this exercise.
The fossil record is almost exclusively
limited to the resistant remains of cyst walls
(see earlier comments on Dinogymnium for
a possible exception). Thus one is faced with
comparing a lot of information regarding the
soft parts and theca of the mastigont phase
of the life cycle with the discarded shells of
another phase or phases. Although it is
fortunate that the tabulation of the theca
is often expressed nearly wholly or in part
on the walls of the cyst either as lines
("paratabulation") or arrangements of
projections or other ornamentation, this is
found mainly in the fossil and living gonyaula-
coids, peridinioids (reviewed by Lentin and
Williams, 1975) providing little information
on thecal tabulation on their cyst walls (some
species of Palaeoperidinium being a striking
exception, even intercalary bands and
information on probable overlap being visible
as a negative imprint on the inside of the cyst
wall: Gocht and Netzel, 1976). No prorocen-
troid fossils are known but they might n o t be
recognisable using the palynological criteria
of today (Loeblich III, 1976a).
Many (most?) living dinoflagellates do not
appear to produce fossilizable cysts and some,
such as Protogonyaulax tarnarensis and
Peridinium faeroense (Dale, 1977, 1978;
Turpin et al., 1978) produce cysts which
would not be confidently assigned to dino-
flagellates if found as fossils, probably being
referable to the "acritarchs".
When these facts (and others noted by
Taylor, 1978) are combined with the un-
doubted "holes" resulting from incomplete
study, it is remarkable that so much has been
gleaned so far from the study of fossil dino-
flagellates. Comparisons between numbers
of taxa present in past strata and today are
largely invalid due to the differing taxonomic
practices of neontologists and palynologists.
As Dale (1978) has put it: "Cysts are
98
probably 'over classified' in the paleontologic-
based system" and "Thecate dinoflagellates
are probably 'underclassified' in the biologic-
based system", resulting in a much greater
formal recognition of taxa, particularly
genera, for similar degrees of morphological
difference in the former system.
The earliest critically accepted record of a
dinoflagellate is now that of Arpylorus in the
Silurian (recently reviewed, with a re-exami-
nation of material, by Sarjeant, 1978). The
paratabulation on this form is very difficult
to resolve although, if Sarjeant's interpreta-
tion of girdle position is correct, the archeo-
pyle (excystment aperture) is anterior inter-
calary in position, a peridinioid-like feature.
The symmetry of the patterning cannot be
satisfactorily determined.
In the Late Triassic other undoubted dino-
flagellates are known, several of these,
including Suessia and Rhaetogonyaulax
having a larger number of paraplates than the
plates of most recent gonyaulacoids or peri-
dinioids. Despite its name Rhaetogonyaulax
does not resemble a gonyaulacoid as recogniz-
ed here, lacking the torsion typical of most
of the latter; having numerous subequal
anterior intercalaries alternating with the
precingulars, and having seven precingulars
and postcingulars. Dapcodinium, which has
also been found in the Late Triassic,
resembles Rhaetogonyaulax in epithecal
features but has a gonyaulacoid-like distortion
of the hypothecal paratabulation, raising the
interesting possibility of an AA symmetry
(Evitt, pets. comm.), not known in living
dinoflagellates {with the possible exception
of Peridiniella}.
The first possible dinophysoids, referred to
as species of Nannoceratopsis, have been
found in the Early Jurassic. However, as
noted earlier, although there are many
striking resemblances to modern dinophysoids,
including general form and the position of a
main dorso-ventral sagittal suture, the
epitheca possesses an unusually large number
of plates similar in pattern in some ways to
peridinioids.
From the Cretaceous onward there are
numerous fossils, including undoubted peri-
dinioids (e.g. Deflandrea) and gonyaulacoids
{e.g. Gonyaulacysta). The earliest Heteraula-
cus-like pattern can be seen on some highly
ornamented Cretaceous (Albian) cysts such as
Dinopterygium, forms looking most like
modern Heteraulacus, such as Heteraulacysta,
occurring in the Early Tertiary {e.g.
Morgenroth, 1966: Eocene).
If one accepts the published dinoflagellate
fossil record as reasonably complete, with the
earliest stratigraphic records closely reflecting
the origin of particular tabulational types,
then not only is there little support for the
sequences suggested in the present paper, but
there are inversions of many of the postulated
sequential events (G. Eaton, pers. comm.).
For example Suessia, one of the earliest
recorded with its many paraplates, could be
looked on as Woloszynskia-like, i.e. transi-
tional gymnodinoid. Peridinioid-like appears
before gonyaulacoid-like. Heteraulacus-like
patterns (closest to the basic model here) only
appear in the record later, as do the only
possible dinophysoids, and prorocentroids are
not there at all. The "tree" on Plate 1 is
upside down! Large number of paraplates
seem to precede smaller numbers, the exact
opposite to the proposed subdivision, rather
than fusion, suggested here.
Even accepting the limitations already out-
lined earlier, it might seem a form of willful
perversion to maintain the probability of the
sequences proposed here. Earlier it was
admitted that the morphoclines seen today do
not permit certainty as to the direction of
change. However there are several critical
factors which, this author believes, open up
the possibilities and suggest that the record
is grossly incomplete and consequently mis-
leading (see also Taylor, 1978).
Firstly, although most neontologists do not
accept the proposal that dinoflagellates are
intermediate between prokaryotes and
eukaryotes {therefore having evolved before
any of the latter) they are still considered to
be one of the most primitive euharyotic

groups, or the most primitive eukaryotes,
depending on whether one rates nuclear
features more significant indicators of
primitiveness than chloroplast features or
lack of flagella (Loeblich III, 1976a; Taylor,
1976, 1978). Even the cytoplasmic ribosomal
R N A shows sign o f being primitive, the larger
subvnit having a smaller molecular weight
than that of other eukaryotes (Gressel et al.,
1975). Consequently they are thought to have
evolved before most protists, including those
thought to have given rise to the macrophytic
green or brown algae, land plants or meta-
zoans. This is utterly inconsistent with their
Silurian origin as suggested by the fossil
record, for all of the latter groups were
apparently well developed by the Late
Precambrian or Early Cambrian, 500 to 600
million years ago.
There is a record of a Precambrian dino-
flagellate, Zosterosphaera tripunctata, in the
literature, Schopf {1968) having tentatively
assigned a microfossil from the Bitter Springs
formation to this group. However this attribu-
tion has n o t been generally accepted by
palynologists and there is nothing distinc-
tively dinoflagellate-like in this spherical b o d y
with a few pore-like markings and internal
projections. It would probably be termed an
acritarch by most recent authors.
This raises the second major caveat. There
are many acritarch records earlier than the
Silurian, including some that are suggestive of
dinoflagellates but with too little to go on to
be certain (e.g. Cymatiogalea; Gorka, 1969),
and quite a few Precambrian forms. It has
been noted several times earlier than the
cysts of Protogonyaulax tamarensis and
Peridinium faeroense would not be definitely
attributable to dinoflagellates using the
current, properly conservative criteria of
today, if fossilized. This opens the strong
possibility that some "acritarchs" are actually
fossilized dinoflagellate cysts, a possibility
which becomes a probability when the
apparent primitiveness of the group is con-
sidered relative to the ancestors of groups
with good Cambrian fossils. If gonyaulacoids
99
or peridinioids can produce acritarchous
cysts, what value do first paratabulational
records have relative to the emergence of
these groups? Admittedly, the earliest dino-
flagellates could have maintained an
athecate, d e s m o k o n t form for a long time
before evolving a theca with distinct tabula-
tion, but there is no reason to assume that
the formation of fossilizable cysts was
correlated with this in any way, and
especially not the fortuitous "reflection"
of the tabulation as discernable marks on
the cyst wall.
Alternative arrangements within the group
The " t r e e " in Plate 1 gives an abbreviated
but still overcrowded picture of the arrange-
ment of the living members considered most
reasonable here. Ironically, despite more than
90 years of further study, it is very similar to
Berth's (1881a,b) first hypothetical scheme
of evolution for the group, proceeding from
desmokonts to dinokonts, with gymnodinoids
considered more advanced than those with
heavier thecae and fewer plates. BiJtschli
(1885) also held with this view although he
thought that the girdle had shifted from a
posterior position to a more anterior one; the
prorocentroid valves being considered anterior
and posterior, instead of left and right. Bergh
believed that dinophysoids gave rise to the
more advanced forms, and this remains a
possibility although they are given a separate
line here.
There have, of course, been a variety of
other views expressed. They cannot be
detailed here, but can be boiled d o w n to t w o
principal alternatives.
Polyphyletism was suggested by Cavers
(1913). He proposed that Prorocentrum,
Oxyrrhis and Gymnodinium were all on
separate lines (from cryptomonads), the
latter giving rise to the bulk of the dinoflagel-
lates. The demonstration of the fundamental
similarity of ultrastructure in all the principal
groups of dinofiagellates (Dodge, 1971) has
100
made polyphyletism improbable. Neverthe-
less the different nuclear types might be
considered indications of the presence of
several stocks (see discussion by Hollande,
1972).
The most widely held alternative is that in
which the supposed "naked" forms are more
primitive than the heavily armoured forms,
a view more matched to the existing fossil
record (see previous section). The principal
proponents of this view were Kofoid and
Swezy (1921, following Schiitt, 1895). In
order to get around the difficulty of the
prorocentroids (accepted as primitive) having
heavy thecae, they placed them on a separate
line, with Pronoctiluca and Oxyrrhis thought
to be intermediate between the two. They
were more aware than most of the sophisti-
cated organisation of the ocelloid genera,
but recognized them as the end points of sub-
lineages.
In this author's view the gymnodinoids and
their presumed derivatives are relatively
"advanced" dinoflagellates, the use of a
honeycomb of amphiesmal vesicles for peri-
pheral strength being sophisticated rather
than primitive. It must be admitted that their
elaborate diversification, including ocelli,
nematocysts, cytostomes, tentacles, con-
tractile wings, etc., could be explained in
terms of having been in existence for a longer
time.
The phyletic position of dinoflagellates
The two groups most frequently linked
with the dinoflagellates by early authors,
such as Bergh (1881a,b), Bi~tschli (1885)
and Carets (1913), were the ciliates and
cryptomonads.
The ciliate link undoubtedly resulted from
the early misapprehension that the girdle
contained cilia (hence the name "Cilio-
flagellds" used by Clapardde and
Lachmann, 1859). Once corrected by Klebs
(1883) the argument was weakened. The
multinucleate condition of Polykrikos was
still considered a possible link between the
two by Cavers (1913), but doubted by
Kofoid and Swezy (1921). The strongest
indication of an affinity is that indicated by
the resemblance between the ciliate cortex
and the dinoflagellate amphiesmal structure
(see section on structure), and it is on this
basis that Corliss (1975) and Taylor (1976b,
1978) suggested a close relationship between
the two. There is no sign of the dinokaryotic
condition in ciliates, the chromosomes having
interphasic dispersal and the spindle being
intranuclear, although both groups can have
very large amounts of DNA per cell. The
mitochondrial architecture is similar in the
two groups, both having tubular cristae.
Dinoflagellate oblique fssion seems somewhat
similar to the unusual transverse fission of
ciliates, other protists having longitudinal
fission, but the fission furrow begins posteri-
orly in dinoflagellates,as in other flagellates.
Dinoflagellates and cryptomonads were
grouped together in the division Pyrrhophyta
by many earlier phycologists (e.g. Pascher,
1914). However, the closeness implied by this
grouping is not supported by detailed
structural or biochemical analysis. They are
similar in the possession of hairy flagella
(although the hairs are of a different type),
internal walls (of different composition),
possession of chlorophyll c2 and the produc-
tion of starch as a storage, but differ in
nuclear, chloroplastic (structure and non-
chlorophyllous pigments), mitochondrial and
trichocyst features.
Similarly a grouping with euglenoids (as
the subkingdom Euglenophytaria Dillon,
1963) is based on some shared characters:
permanently condensed chromosomes and a
persistent nucleolus in most members, hairy
flagella with secondary banded, fibrous
supportive structure (the striated strand of
dinoflagellates and paraflagellar rod of
euglenoids), internal walls, three-membraned
envelope of the chloroplast, thylakoid groups
in threes and some similaritiesof mucocyst
or trichocyst structure but they differ in
pigments, storage products, presence of his-

tones and internal mitotic spindle in eugle-
noids, wall composition, mitochondrial
structure and other features.
A link to radiolaria has been suggested on
the basis of the topological similarity of the
radiolarian capsule and the theca of dino-
flagellates (Hollande et al., 1970), a mitosis
superficially resembling that of Syndinium
but with an intranuclear spindle, and the
presence of siliceous endoskeletons in some
dinoflagellates. The resemblance between the
mitotic process of dinoflagellates and hyper-
mastigid flagellates has been noted earlier in
this text.
The apparent primitive features of the
nucleus suggest that, whatever their nearest
relatives might be, the dinoflagellates occupy
a position close to base of the eukaryotic
radiation, but it is also evident that they are
a highly specialized group. Taylor (1976b,
1978) has placed them at the base of the
Chromophyte Series. On the basis of bio-
chemical features only Ragan and Chapman
(1978) placed them in a similar position but
noted that, due to anomalies, "any phylo-
genetic positioning will invite criticism".
Conclusions
The dinoflagellates are a group of striking
diversity, exhibiting some of the most primi-
tive and yet also some of the most sophisti-
cated structure to be found among the
protists. Despite this great variety, certain
major features can be postulated to have
arisen by particular sequences of events,
deduced from comparisons with other flagel-
lates and the surprisingly large number of
gradients of structure shown by living forms.
The principal events postulated are listed
below.
(1) The flagellahave shifted from the apical
position (relativeto the direction of motion)
c o m m o n to most flagellatesand the desmo-
kont dinoflagellates,to a lateral insertion,
accompanied by the formation of surface
furrows. The transverse flagellum became
101
ribbon-like even in the desmokonts (thought
to be the most primitive dinoflagellates) and,
together with the cingulum (girdle groove),
has become a functional unit which not only
turns the cells, but also propels if forward.
(2) The cellulosic cell wall (theca) of the
motile stage is always intracellular, having
been formed within closed vesicles. It has
been transformed from paired, thick lateral
valves plus a field of minute but orderly
platelets around the two flagellar pores
(prorocentroids), to more subdivided lateral
valves plus a girdle and sulcus in which the
flagella both arise from one pore (dinophy-
soids). A further development may have been
the subdivision of the theca on an essentially
radially symmetrical plan, with six longitu-
dinal sectors sub<iivided into five latitudinal
series of plates (two versions of this, gonyau-
lacoids and peridinioids, due to differences in
flagella insertion or orientation). Distortion
and subdivision of plates has occurred fre-
quently, loss of sutures being more rare. The
epithecal pattern has been less conservative
than the hypothecal, and the left side more
subject to change than the right. Finally, in
gymnodinoids peripheral strength has been
achieved by proliferation of the vesicles into
a honey-comb-like configuration. The greater
the number of vesicles, the thinner the thecal
plates (a rule which applies to most dino-
flagellates) and they may be lost entirely in
some. Secondarily a continuous fibrous
layer or layers (the pellicle) has been laid
down beneath the vesicular layer in some, and
can serve for strengthening of the motile cell,
the immediate wall of ecdysal cysts, or
probably, can differentiate into the resting
cyst wall.
(3) Endogenous cysts (non-motile stages
with continuous walls) have been developed
for various functions, including asexual
ecdysal (pellicle) cysts in which the theca is
shed. Resting cysts, with resistant, thick walls
and excystment via a precisely positioned
aperture, the archeopyle, are hypnozygotes
in some, if not all cases, but are not formed
by many dinoflagellates. Calcification of the
102
cyst wall has occurred in some peridinoid
taxa. Silicification of cyst walls is known only
from fossil forms and may not be a primary
phenomenon. In some a cyst stage has
become dominant in the life-cycle (vegetative
cysts). Secondary cysts may be produced
before the motile stage is formed. Exogenous
"cysts", which are ephemeral, gelatinous,
protective coverings, may precede gymno-
dinoid division, or the formation of a more
substantial wall. Sexuality seems to be present
in many species although is often cryptic.
Therefore its apparent absence from members
postulated to be more primitive may be
deceptive.
(4) The internal cell organization is built on
the same basic plan as that of other eukaryo-
tic flagellates. The type of flagellar dimor-
phism associated with surface grooves,
pusules, and fibrillar, continuously con-
densed chromosomes are distinctive. The
most common nuclear condition (dino-
karyotic) exhibits some prokaryote-like
features which might indicate great primitive-
ness. Other features thought to be primitive
are shared with some other eukaryotic groups
possessing "cryptomitosis" (persistence of the
nuclear membrane). The totally external
spindle is unusual but occurs also in tricho-
monad and hypermastigote flagellates. Devia-
tions from the dinokaryon have developed
principally among the parasitic and nocti-
lucid members (all probably gymnodinoid
derivatives}.
(5) Loss of photosynthesis seems to have
occurred in most lineages, primitive forms
being generally photosynthetic and more
derived forms not. If the chloroplasts were
acquired by symbiosis then this occurred
before the radiation of the main lineages,
although fucoxanthin-containing chloroplasts
appear to have been secondarily acquired
through recent symbioses. The pigment
spectrum resembles the "chromophyte type",
with peridinin a dominant xanthophyll
unique to the group. Starch formation
resembles that in the chlorophytes (except
that it is extrachloroplastic). A 4a-methyl-
sterol, dinosterol, is so far known only from
members of the group.
(6) Common parallelisms found in the
various lineages are: "sinistrality" (greater
development of structures on the left side
of the cell}; the production of horns or
flattened projections, apical pore formation,
list elaboration, flattening of the body,
torsion (most commonly left-handed),
inflation of the body by vacuoles, chain
formation, predominance of a non-motile
stage, multicellularity, phagotrophy, and
parasitism.
(7) Notable developments restricted to
only one or a few sublineages are: loss of
the girdle plates; formation of a chamber
from the girdle lists (for cyanophyte
symbionts?); the production of an internal
siliceous skeleton; the development of ocelli
and nematocysts; formation of a coenocyte-
like condition in motile cells by the fusion of
individuals and reduction in the number of
nuclei; movement of either the whole body or
extensions of it by microfibrillar bundles and
the use of body movements for medusoid-like
locomotion and multicellularity.
(8) The fossil record appears to be
extremely incomplete, judging by the
apparent primitiveness of the group. Some
"acritarchs" are probably dinoflagellate cyst
remains.
(9} There appear to be two major lineages
within those genera usually attributed to the
order Peridiniales: peridinioids and gonyaula-
coids. Although the number of plate series
and general arrangement is similar, the two
can be fundamentally distinguished by an
analysis of their type of symmetry relative to
the flagellar insertion. A new order has been
proposed for the gonyaulacoids (see below}.
Systematic appendix
Diagnosis for the Order Gonyaulacales ord.
nOV.
Dinoflagellates with five principal lati-

t u d i n a l series o f p l a t e s in w h i c h t h e p o l a r
p a t t e r n , relative t o t h e flagellar i n s e r t i o n , is
of the YA type.
Dinoflagellate ordinatione symmetriae
thecalis YA fundamenti (ad insertionem
flagellarem pertinentis ) distinctae.
New combination
Plectodinium miniature (Kofoid and
Swezy) comb. nov.
B a s i o n y m : Cochlodinium miniature K o f o i d
a n d S w e z y 1 9 2 1 , p. 3 7 2 , t e x t Fig. G G 6,
Plate 10, Fig. 107.
Syn.: Plectodinium nucleovolvatum
Biecheler, 1 9 3 4 .
K o f o i d a n d S w e z y ( 1 9 2 1 ) i l l u s t r a t e d this
t a x o n u p s i d e d o w n , w i t h i n c o r r e c t flagellar
de eails a n d this is w h y t h e i d e n t i t y o f t h e t w o
t a x a was n o t p r e v i o u s l y recognised. T h e apical
spinelets a n d n u c l e a r capsule are clearly
s h o w n in K o f o i d a n d S w e z y ' s figures.
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