Is the archeopyle of Tuberculodinium vancampoae (Rossignol) (Gonyaulacales, Dinophyceae) on the hypocyst?

10 Pages·1998·3.4 MB·English

by  Kazumi Matsuoka

©Paleontological Research, vol.2, no.3, pp.183-192, 8Figs., September 30, 1998
by the Palaeontological Society of Japan
Is the archeopyle of Tuberculodinium vancampoae (Rossignol)
(Gonyaulacales, Dinophyceae) on the hypocyst ?
KAZUMI MATSUOKA1 PORNSILP PHOLPUNTHIN2 and YASUWO FUKUYO3
,
department of Marine Biology, Faculty of Fisheries, Nagasaki University, 1-14, Bunkyo-machi, Nagasaki 852-8521, Japan.
department of Biology, Faculty of Science, Prince of Sognkhla University, Hat-Yai 90112, Thailand.
3Asian Natural Environmental Science Center, University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan.
Received 14 February 1998 Revised manuscript accepted 22 June 1998
;
Abstract. The archeopyle type in modern dinoflagellate cysts is classified into the following saphopylic,
theropylic and cryptopylic types. Within the saphopylic type, Tuberculodinium vancampoae (=cyst of
Pyrophacus steinii) is the only species generally accepted as having an archeopyle developed on the
hypocyst. However, the archeopyle type of this species has been alternatively explained as being
precingular ratherthan hypocystal. New observations have led usto conclude that the archeopyle of T.
vancampoae is neither hypocystal nor precingular, but epicystal in type. Specimens ofthe hypnozygote
ofP. steiniirecovered ina planktonsamplefromOmura Bay,WestJapanshowarcheopylesuturesformed
neitheron antapical norprecingularsidesbutontheapical sidewheretheyaretopologicallyrelatedtothe
distribution of large and barrel-shaped processes and remaining thecal plates that overlap the
hypnozygote. The hypnozygotes of P.steinii, wrapped in their planozygotic thecae, were carefully
observed at germination during an incubation experiment. One of the living hypnozygotes was still
enveloped by the thecae of the planozygote. Then, several weeks after the encystment, a motile cell
germinatedfromthe hypnozygotethrough oneopening (=archeopyle)formed ononeflatside. Sincethe
thecae of the planozygote was still attached to the surface of the hypnozygote, the position of the
germinationsitewaseasilydeterminedwith relationtothethecal plates. Abovethearcheopyleconsisting
oftwoparaplates,theapicalpore platewithtwofurrowswasobserved. Itisclearthatthearcheopylewas
formed not on the antapical but on the apical side.
Key words: Archeopyle, dinoflagellate cyst, Dinophyceae, hypnozygote, planozygote, Pyrophacus, Tuber-
culodinium
Introduction proposed in the cyst genus Caligodinium by Manum and
Williams (1995) based on the careful observation and more
Forthe identification of both modern and fossil dinoflagel- rational interpretation of the topological relation of each
late cysts, the archeopyle is one of the important character- paraplate. Another example of a hypocystal archeopyle
istics(e.g., Evitt,1963,1985). Thearcheopyletype in modern (probably involving loss of postcingular paraplates) ar-
dinoflagellate cysts is classified into saphopylic, theropylic cheopyle was introduced for siliceous fossils of some
and cryptopylictypes inthe relationtothe plateseriesforthe species of Peridinites (=a synonym of Lithoperidinium
armored group and position for the unarmored group according to Lentin and Williams, 1993), Peridinites oamaru-
(Matsuoka, 1988). The saphopylic archeopyletype is devel- ensis and P.parvalus, with semidiagramatic illustrations by
oped in mostgonyaulacoid and protoperidinioid cystsexcept Dale (1978). However, Harding and Lewis (1994) concluded
for an unclear type observed in the cysts of Alexandrium that fossil Peridinites is not a cyst but a silicified theca and
species and Gonyaulax verlor. The other modern cysts in therefore the opening observed on the hypotheca is not a
these groups are apical, intercalary, precingular, epicystal or real germination apparatus(=archeopyle). Forthe moment,
some combinations thereof. Only one example of a the hypocystal archeopyle seems to be only a hypothetical
hypocystal archeopyle has been generally accepted, this interpretation for Peridinites.
being Tuberculodinium vancampoae (Rossignol) (=cyst of Following Wall and Dale's (1971) proposal for a hypocystal
Pyrophacus steinii steinii and P. steinii vancampoae) by Wall archeopyle in P. stenii cysts, there have been no effective
and Dale (1971) and followed by Matsuoka (1985). and persuasive studies on the hypocystal archeopyle type in
A hypocystal archeopyle in fossil dinoflagellates has been modern dinoflagellates. We will prove that the archeopyle
+
184 Kazumi Matsuoka et al.
of T. vancampoae is nothypocystal butepicystal onthe basis mopsis, P. ? vancampoae by Rossignol (1962). Later this
of observations for plankton and incubated specimens of P. species was transferred to Tuberculodinium, then a newly
steinii. erected dinophycean genus byWall (1967). Intheemended
diagnosis for Tuberculodinium vancampoae, Wall (1967)
Previous study on the archeopyle type of mentioned that the archeopyle of this species is a large
Tuberculodinium vancampoae compound type consisting of precingular and anterior inter-
calary paraplates. Drugg (1970) also interpreted the ar-
The fossil cyst of Pyrophacus steinii (=Tuberculodinium cheopyle of fossil Tuberculodinium as precingular.
vancampoae) was first described from the Pleistocene of Then in1971, Wall and Daleconcludedthatthearcheopyle
Israel as a new species questionably assigned to Pterosper- of this cyst is not compound precingular but hypocystal
Table1.
Wall Drugg Wall & Dale Stover & Evitt Wrenn & Damassa
This study
(1967) (1970) (1971) (1978) (1989)
Material fossil cysts fossil cysts living literature fossil cysts livingvegetativecells,
hypnozygotes planozygotes and
incubated hypnozygotes
Compression dorso-ventrally dorso- anterio- anterio-posterior dorso-ventral cyst anterio-posterior
direction in ventrally posterior rotated 90 degree
cysts within the
planozygose
Archeopyle type compound precingular hypocystal compound precingular compound
; ; ;
precingular antapical epicystal
anterior
intercalary
Wall features not mentioned notintratabular not mentioned intratabular not mentioned ?
9" 1" =
T°"
,
11"
y)"
1
- 9„
*-?« O
b
50jim
Figure1. Plate tabulation in vegetative cell, a; apical plate series, b; precingular plate series, c; apical
pore complex (ape)and 1', d; postcingular plate series, e; posterior intercalaryandantapical plate series, fandg:
sulcal plates, as: anterior sulcal plate, ra: right accessary sulcal plate, la: left accessary sulcal plate, aas:
anterior accessary sulcal plate, rs: right sulcal plate, Is: left sulcal plate, ps: posterior sulcal plate, fp: flagellar
pore.
Archeopyle of Tuberculodinium vancampoae 185
based on the result of cyst incubation experiments on P. were picked up with a micropipette and then mounted on a
steinii. This explanation was followed by Matsuoka (1985) slide glass with glycerine jelly. These hypnozygotes were
based also on the incubation method. Stover and Evitt examined under the interference optics of a Zeiss Axiphoto
(1978) suggested that Tuberculodinium has an antapical microscope.
rather than hypocystal archeopyle. However, the possibility Surface sediments containing living cysts ofP. steiniiwere
that the archeopyle type of Tuberculodinium is not hypo- collected from Omura BayandTokyo Baywith aTFOgravity
cystal but precingular was raised by Wrenn and Damassa corer in 1990. The top 2cm of the sediments was cut and
(1989). removed to a refrigerator below4 until starting the incuba-
Thus, the archeopyle type of 7. vancampoae remains tion experiment. The material was sonified and sieved with
unclear and the subject of discussion (see Table1). stainless screens of120^m and 20pim in pore size, and the
living cysts of P. steinii were picked up to in oculate in a
Material and method culture dish with SWII medium. The living cysts were
cultured under20°C,about100^mol photons • rrr2 • s_1 and
A plankton sample was collected with a net haul in June 12 hours —12 hours cycle. The culture was continued until
of1983from OmuraBay, WestJapan,and preservedwith5% one whole life cycle of this species from vegetative cells to
formalin. Several specimensofthe hypnozygoteofP. steinii planomeiocytes via planozygotes and hypnozygotes, was
*S
^Hfj^
\rf{$Tf*Aw^
\ T'/C'-' Vls{
50^m
Figure2. Hypnozygote involved bythecae ofplanozygote ofPyrophacus steinii in plankton sample collected
from Omura Bay on Juneof1990. A serial photographsfrom apical surface(a)toantapical surface(i). a; apical
pore complex (black arrow) and 1' of the planozygote. b and c; three paraplates (?) corresponding to the
archeopyle which has already appeared before germination on the surface of hypnozygote (white arrows), and
tprheecciangouflaprlapnroozcyegsostees(b(lbalcakckararrorwo)wsa),nd edc;toepnlharraggemmeofnthyopfnotzhyegoatrech.eopgyl;es.ulceus; oopftipclaalnoczryogsostese(cbtliaocnk,arfro;wh)yapnod-
postcingular processes of hypnozygote (white arrow), h; antapical processes distributing circularly (white arrows)
and sulcus of planozygote (black arrow), i; antapical surface of planozygote.
186 Kazumi Matsuoka et al.
Hypocyst
Epicyst
Sulcus
Apicalpore
"Archeopyle
Epitheta Hypotheca
Figure3. Illustrationofaplanozygotecontainingahypnozygote, collectedfromOmuraBay, westJapan,June
1990. A Epithecaand epicyst showing archeopyle sutures, B Hypotheca and hypocyst, the same specimen of
; ;
Figure2.
VI
, ' > '
V
H
. f
.
50um
Figure4. Hypnozygote involved bythecaeof planozygote ofPyrophacus steinii in plankton sample collected
from Omura Bay on June of 1990. Serial photographs from apical surface (a) to antapical surface (i). a; apical
pore plate(blackarrow), b epithecaof planozygoteand 1' plate(blackarrows), c apical processeswith linear
; ;
distribution (white arrows), d precingular processes (white arrows), e cingular plates of planozygote (black
; ;
aprlraonwo)zyagnodteecatnodphhryapgomtheofcahy(pblnaoczkygaorrtoews()w,hithe;ar3r"o"w)(,blafc;kpaorsrtocwi)ngaunldaranptraopciecsaslespr(owcheistseesarrdoiwsst)r,ibutgin;gscuilrccuulsarolfy
(white arrows), i; posterior intercalary of plate planozygote (black arrow).
Archeopyle of Tuberculodinium vancampoae 187
completely observed. In particular, one specimen which processes positioned circularly (Figures5g, h, i). The plate
had a well preserved archeopyle structure was carefully formula ofthis planozygotewas7', 11",13c,13'", 4p, lap, and
examined under interference optics of a Nikon Biophoto 3'", and the processformulaofthis cystwas5(3+2s)'-t-2@,
microscope. 11", 0c, 10'", and 3""+3s.
Since the number of plates in P. steinii is (Figure1) very
variable, there have been several different interpretations of Observation on the transformation from planozygote to
its expression. In this paper, we follow the interpretation of hypnozygote during incubation (Figure7)
Matsuoka (1985). Clonal cultures of P. steinii were established by a single
cell isolation from net-haul samples at Yokohama Umizuri-
Results sambashi in innermost Tokyo Bay on June, 1990. During
the clonal cultureforthisspecimen, both sexual and asexual
Plankton specimens of hypnozygotes (Figures2,3,4) reproduction occurred. Sexual reproduction started to
A few immature resting cysts were collected in plankton result in small and round thecate cells (male gametes).
samples from Omura Bay. These cysts were filled with Female gametes were not morphologically differentiated
fresh protoplasm and surrounded the planozygotic theca, from normal vegetative cells in plate formula and size. By
clearly demonstrating a morphological relation between the sexual fusion of male and female gametes, a planozygote
planozygote and resting cyst. It is therefore easy to estab- was produced and was morphologically similar to vegetative
lish the orientation of the thecal plate and process distribu- cells except for its larger cell size. After one to two days
tion on the cyst. activeswimming, the planozygote stoppedmoving, and sunk
Theepithecaofthe planozygotecould easilybeconfirmed to the bottom of the culture chamber. The hypnozygotes
by the presence of the apical pore plate, seven apical, and were produced as a result of protoplasm contractions to
eleven precingular plates (Figures2,3a). Beneth the apical approximately1/5 oftheoriginalvolume. Afterdevelopment
pore plate, three large, barrel-shaped processes and a of the exospore, many processes were formed between the
certain space were noticed on the cyst surface (Figures2b, exospore and the surface of the protoplast (mesospore).
d). A polygonal outline similar to some plate boundaries These processes were barrel-shaped and identical to those
confined this space. One row consisting of ten large and previously observed in fossil forms. This hypnozygote was
barrel-shaped processes ran along the shoulder (Figures2b, contained within the theca of the planozygote (Figure7).
4d). Severalweeksaftertheencystment, amotilecellgerminated
The opposite side of the hypnozygote contained the from the hypnozygote through one opening (=archeopyle)
sulcus, and thirteen postcingular, three posterior intercalary, formed on one flat side. As the theca of the planozygote
and three antapical plates were observed (Figures2f, 3b). was still attached to the surface of the hypnozygote, the
Beneth this hypotheca, eleven large barrel-shaped position of the germinated side was easily determined with
processes were formed on the shoulder of the cyst. Eight relation to the thecal plates. The archeopyle consisted of
large barrel-shaped processes were circularly distributed on two paraplates, and above it, an apical pore plate with two
this cyst surface (Figures2g, h). furrows was observed (Figure5c).
The plate formula of the planozygote shown in Figure2
was demonstrated as 7', 11", 13c, 13'", 3p, 3"" and 5s, while Discussion
the process formula on the cyst would be described as 3'+
3@, 10", 0c, 10'" and 8"" (@ paraplates consisting of the Position and type of archeopyle
:
operculum). Wall (1967)established anewgenus Tuberculodinium after
revising Pterospermopsis? vancampoae Rossignol and
Observation of empty hypnozygote surrounded by the emending the species diagnosis so that the archeopyle
planonozygote (Figures5,6) corresponds to a combination of precingular and intercalary
Some hypnozygotes used for our study on the life cycle paraplates. Drugg (1970) also considered the archeopyle of
remained within the planozygotic theca and its wall even Tuberculodinium to be precingular with the number of
after excystment (Figure5). Figure6 shows the mor- detached opercularplates beingvariable in differentspecies.
phological features of both planozygote and hypnozygote. Later, Wall and Dale (1971) observed the cysts of P. steinii
The planozygote had one apical pore (Figure5a), seven and P. vancampoae, which now Balech (1979) and Matsuoka
apical and eleven precingular plates. On the cyst surface (1985) consider to be two subspecies ofP. steinii, and noted
just beneaththisepitheca,therewasan archeopyle probably that the archeopyle is hypocystal and that the number of
corresponding to two paraplates (Figure5c) and five larger paraplates comprising the operculum variesfrom twotofour.
barrel-shaped and three small, simple spherical processes However, this conclusion was not based on direct observa-
distributed on one shoulderofthe peripheral side(Figures5d, tion of germinated hypnozygotes, but on mostly theoretical
e). grounds. The interpretation given by Wall and Dale (1971)
The hypotheca consisted of thirteen postcingular, three was as follows: Four parallel rows consisting of large and
posterior intercalary, three antapical, thirteen cingular, and barrel-shaped processes on the cysts were considered to
fivesulcal plates(Figures5j, k, I). Onthecystsurfaceofthis represent apical, precingular, postcingular and antapical
side, eleven large and barrel-shaped processes were locat- plate series of the thecate form respectively. Ofthese four
ed on the shoulder, and six large and barrel-shaped rows, one contained two to five rectangular to polygonal
Kazumi Matsuoka et al.
Archeopyle of Tuberculodinium vancampoae 189
Epicyst Hypocyst
/ Sulcus
Apicalporeplate
\rclicopylc
Cingulum
Epitheca Hypotheca
Figure6. Illustration of a planozygote containing an empty hypnozygote after germination in culture. A
;
Epitheca and epicyst showing archeopyle sutures, B Hypotheca and hypocyst, the same specimen of Figure4.
;
paraplatesformingthearcheopylewhich resembled posterior (1995).
intercalary and sometimes additional posterior plates of the The specimens recovered from the net samples of Omura
thecate cell. The processes opposite to this row were Bay also demonstrated archeopyle formation. These cysts,
circularly distributed and apparentlysimilartothe distribution collected while still floating in surface waters before sinking,
ofapical plateseriesofthevegetativecell. Theseobserva- showed archeopyle structure on the hypnozygote surface
tions led them to conclude that the cysts of P. steinii and P. even though these cellswere filled with protoplasm. These
vancampoae have a hypocystal archeopyle. archeopyles were not yet functional and the opercula were
Matsuoka (1985) found hypnozygotes surrounded by the still in place, butthearcheopylesuturecould neverthelessbe
thecae of planozygotes in a plankton sample collected from traced on the surface. The archeopyle was formed beneth
Omura Bay. However, as the hypnozygotes were filled with the apical pore and apical plates of the planozygote.
protoplasm, he schematically illustrated the general outline According tothe outlineofthe sutures,theoperculaseemed
of one specimen of the planozygote and hypnozygote using to be composed ofthreeorfour paraplates. However, none
the same interpretation as Wall and Dale (1971). of the paraplates morphologically resembled any apical or
Wrenn and Damassa (1989) examined hundreds of fossil precingular plates of the attached planozygote.
specimens of T. vancampoae from latest middle Eocene to The incubated specimens clearly showed the position of
Holocene in detail, and concluded that the cyst morphology an archeopyle, which was also formed beneth the apical
did not correspond to that of the theca that the cyst was pore plate and the apical plate series. In these specimens,
;
dorso-ventrally compressed and that the archeopyle was although the opercula were completely detached leaving
precingular rather than hypocystal. In order to rationalize onlytheiroutline on the surface, the outline did not resemble
this intepretation, Wrenn and Damassa (1989) proposed that either apical or precingular plates of the overlying
during maturation ofthe planozygote, the hypnozygote rotat- planozygote. This observation agrees with the plankton
ed 90° with respecttothe planozygote. Afull description of specimens from Omura Bay.
this interpretation has yetto be published, and unfortunately Under these circumstances, the archeopyle of T. van-
we are therefore unable to evaluate their observations in campoae (=hypnozygote of P. steinii) is formed on the
detail. However, we never observed the hypnozygote to epicyst, but it is very difficult to determine the type exactly.
rotate from earlyto matured stage in the planozygote(Figure It should be called epicystal and compound rather than
7). According to our observations, we can also conclude hypocystal or antapical.
that this is unlikely as suggested by Manum and Williams
Figures. Theca of planozygote and hypnozygote after germination. Serial photographs from apical view (a) to
antapical view(I), a: apical pore plateand apical plates(3', 4', and 5' ; blackarrow), b: precingularplates(blackarrows),
c: large apical process (small white arrows) and archeopyle (large white arrow)formed on the surface of hypnozygote. d:
large apical processes (white arrows) and endospore remaining in the cavity of the hypnozygote (black arrow), e: large
precingular processes (blackarrows), f: optical cross section of hypnozygote. g: cingular plates, h: large postcingular
processes, i: 1"" (black arrow) and antapical processes distributied circularly (white arrows), j: 3"" (black arrow), k:
posterior intercalary plates (black arrow). I : additional posterior intercalary plates (black arrow).
-
190 Kazumi Matsuoka et al.
Lateral view
Figure7. Hypnozygote producedwithin aplanozygoteofPyrophacus steiniiduringthe incubationexperiment.
APS anterior flattened polar surface, UC upper corner of flattened polar surface, LC lower corner of flattened
: : :
poar surface, PPS posterior corner of flattened polar surface.
:
Intratabular structure on the hypnozygote on the cystand no paraplates exceptfor archeopyle sutures
Stoverand Evitt(1978)mentioned that intratabularfeatures which sometimes showed a polygonal outline. As with
in T. vancampoae arearranged in longitudinal rowsof barrel othergonyaulacoid cysts,the numberoflarge, barrel-shaped
shaped processes and are absent in the equatorial area. processes is alwaysfewerthan that ofthecal plates on both
Drugg (1970) considered intratabularfeaturesto be absent in vegetative cells and planozygotes. There was no reflection
in twofossil species, T. vancampoae and T. rossignoliae, and of the cingulum, which was always shown by the space
that exceptforthe archeopyle, no parasutural features were between two rows of large, barrel-shaped processes cor-
observed. However, Wrenn and Damassa (1989) demon- responding to pre- and postcingular plate series. The
strated an intratabular distribution as suggested by one operculum detached from the cystdoes notcorrespond with
barrel-shaped, large process placed in the center of one any apical and precingular plates of vegetative cells and
paraplate clearly bounded by parasutural features in fossil planozygotes in shape and position.
Tuberculodinium vancampoae. The outline of these para- Forclear understanding howthe processesare developed
plates closely resembles each opercular piece. during maturation from the planozygote to hypnozygote, this
AccordingtoWall and Dale(1971)and Matsuoka(1985),the progress should be continuously observed during incubation
modern cysts of Pyrophacus steinii, including P. steinii van- as was done on Lingulodinium polyedrum by Kokinos and
campoae, do not show any paraplate features like those in Anderson (1995).
fossil specimens. Futhermore, there were no parasutures
Archeopyle of Tuberculodinium vancampoae
191
Saphopylic type
Apical
Epicystal
Intercalary Precingular
Apical/Intercalary/Precingular
COMBINATION
Theropylic type
Transapical
Cryptopylic type
Tremic Chasmic
Figure8. Archeopyle types developed in modern dinoflagellate cysts after modification of Matsuoka et al.
(1989) based on the new observation.
192 Kazumi Matsuoka et al.
Acknowledgments Lentin, J.K. and Williams, G.L., 1993: Fossil dinoflagellates :
Index to genera and species 1993 edition. AASP
We are indebted to David Wall and John, H.Wrenn for Contribution Series No.28, viii+856p. American
their kind criticism and helpful suggestion on the archeopyle Association of Stratigraphie Palynologists Foundation.
type of Tuberculodinium vancampoae and also to Rex Manum, S. and Williams, G.L, 1995: Hypocystal arche-
Harland and Martin J. Head for their critical reading of an opyles in the dinoflagellate cyst genus Calligodinium
oeafrlMioernbdruasfth.o,TNhoi.s0p8a6p4er05i9s3parttolythseupspeonritoerdabutyhGorr.and-in-Aid MatssuDtroeukignaig,i.K(.S,Pcha1il9lyl8ne5or)l:oWgCayy,lsltvoael.tnd1D9,atlhpee..c1a8t3Te-r1fa9no0sr.amcstioofnPsyraonpdhaPcruos-
ceedings of thePalaeontologicalSocietyofJapan,New
Reference cited Series, 140, p.240 262.
Matsuoka, K., 1988: Cyst-theca relationships in the
Balech, E., 1979: El genera Pyrophacus steinii Stein (Dino- diplosalid group (Peridiniales, Dinophyceae). Review
flagellate). Physis, sec. A, 38, p.27-38. of Palaeobotany and Palynology, vol.56, p.95-122.
Dale, B., 1978: Acritarchous cysts of Peridinium faeroense Matsuoka, K., Fukuyo, Y., and Anderson, D.M., 1989:
Paulsen: Implications for dinoflagellate systematics. Methods for modern dinoflagellate cyst studies. In,
Palynology, vol.2, p.187-193. Okaichi, T., Anderson, D.M., and Nemoto, T. eds., Red
Drugg, W.S., 1970 Two new Neogene species of Tuber- Tides Biology, Environmental Science, and Toxicol-
: :
culodinium and one of Xenicodinium (Pyrrhophyta). ogy, p.461-479. Elsevier, New York.
Proceedings of the Biological Society of Washington, Rossignol, M., 1962 Analyse pollinique de sédiments
:
vol.83, p.115-122. Quaternaires en Israel. I : Sédiments Pleistocenes.
Evitt, W.R., 1963: A discussion and proposals concerning Pollen et Spores, vol.4, p.121-148.
fossil dinoflagellates, hystrichospheres, and acritarchs, Stover, L.E. and Evitt, W.R., 1978: Analyses of Pre-
I, II. Proceedings of the Natural Academy of Science, Pleistocene organic-walled dinoflagellates. Stanford
vol.49, p.158-164 and p.298-302. University Publications, Geological Sciences, 25, iii+
Evitt, W.R., 1985: Sporopollenin Dinoflagellate Cysts-Their 300p., Stanford, California.
morphology and interpretation, xv+333p. American Wall, D., 1967: Fossil microplankton in deep-seacoresfrom
Association of Stratigraphie Palynologists Foundation, the Caribbean Sea. Palaeontology, vol.10, p.95-123.
Texas. Wall, D. and Dale, B., 1971 : A reconsideration of living and
Harding, I.C. and Lewis, J., 1994: Siliceous dinoflagellate fossil Pyrophacus Stein, 1883 (Dinophyceae). Journal
thecal fossils from the Eocene of Barbados. of Phycology, vol.7, p.221-235.
Palaeontology, vol.37, p.825-840. Wrenn, J.H. and Damassa, S.P., 1989: Tuberculodinium
Kokinos, J.P. and Anderson, D.M., 1995: Morphological vancampoae : A curious reflection of its former self.
development of resting cysts in cultures of the marine Abstract of Fouth International Conference on Modern
dinoflagellateLingulodinium polyedrum (=/.. machaero- and Fossil Dinoflagellates, p.108, Woods Hole, Massa-
phorum). Palynology, vol.19, p.143-166. chusetts, U.S.A.