J. Nannoplankton Res. 30 (1), 2008, pp.1-8 © 2008 International Nannoplankton Association, Inc.
ISSN 1210-8049 Printed by Cambridge University Press, UK

1

New possible hetero-holococcolithophore combinations
within the genus Syracosphaera
Elisa Malinverno
Department of Geological Sciences & Geotechnologies, University of Milano-Bicocca, Piazza della Scienza, 4, 20126 Milano, Italy;
elisa.malinverno@unimib.it

Maria V. Triantaphyllou, Margarita Dimiza
Department of Historical Geology-Paleontology, University of Athens, Panepistimiopolis, 15784 Athens, Greece

Jeremy R. Young
Palaeontology Department, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK

Manuscript received 12th October, 2007; revised manuscript accepted 7th February, 2008

Abstract Two new possible hetero-holococcolithophore combinations are shown: Syracosphaera histrica with S.
pulchra HOL oblonga type and S. molischii with Gliscolithus amitakareniae. In addition, an ambiguous combinationof S. pulchra HOL oblonga type with S. pulchra HOL pirus type is recorded by light-microscope imaging. Although
represented by ambiguous combinations, they potentially document new life-cycle associations within coccolithophores
to add to the complexity of haplo-diplontic coccolithophore stages.

Keywords Coccolithophore, life-cycle, Syracosphaera histrica, Syracosphaera pulchra HOL oblonga type, Syracosphaera molischii, Gliscolithus amitakareniae

1. Intoduction
Coccolithophores are a significant, unicellular phytoplankton group that biomineralise a calcareous skeleton(coccosphere) made of minute plates called coccoliths, themorphology and crystal arrangement of which are the primary basis for coccolithophore identification and classification. Two basic kinds of coccoliths can be distinguishedon the basis of crystal type: holococcoliths, which areformed of minute, identical, euhedral crystals, and heterococcoliths, which are made of larger crystals of variable
shape. Although heterococcolith- and holococcolith-bearing cells were initially regarded as separate species, culture
work (Parke & Adams, 1960; Manton & Leedale, 1969;
Rowson et al., 1986; Houdan et al., 2004; Noël et al., 2004)
has shown that they can undergo transition from one form
to the other (respectively, diploid and haploid), and thus
are considered to be a part of the life-cycle of the same
species. Furthermore, combination coccospheres containing both hetero- and holococcoliths have been recorded
from field-samples (Kamptner, 1941; Lecal-Schlauder,
1961; Kleijne, 1991; Thomsen et al., 1991; Samtleben &Scröder, 1992; Samtleben in Winter & Siesser, 1994; Alcober & Jordan, 1997; Young et al., 1998; Cros et al., 2000;
Cortés, 2000; Cortés & Bollmann, 2002; Geisen et al.,
2002; Cros & Fortuño, 2002; Triantaphyllou & Dimiza,
2003; Triantaphyllou et al., 2004). They are believed to
document the moment of transition between the two lifecycle phases.
The factors causing the transition from one phase to theother are still not well constrained, as both phases are selfreproducing and transitions only rarely occur in culture.
Noël et al. (2004) demonstrated that, in Calyptrosphaera

sphaeroidea, phase transitions in culture can be initiatedby physical or chemical stress, but it is not known if this is
a common pattern in coccolithophores.
Several such combinations are now well established,
due to repeated observations that statistically confirm theirauthenticity. As a consequence, changes in the taxonomic
nomenclature have been proposed (Cros et al., 2000; Jordan et al., 2004), whereby the two species’ names are synonymised and the one having taxonomic priority is adopted
as the name for both life-cycle phases. Various additional
combinations are still unsubstantiated, with the associationof different coccolith types having been documented only
once and/or the specimens being uncertain, possibly resulting from accidental incorporation of coccoliths fromanother species onto a coccosphere during sampling, in a
faecal pellet, or in the water-column (i.e. xenospheres:Young et al., 1997; Young & Geisen, 2002).
Besides the most common, one-to-one hetero-holococcolith combinations, more complex combinations havebeen reported, suggesting relationships of one hetero- with
two or three holococcolith types, for example, Helicosphaera carteri with the former “Syracolithus confusus”
and “S. catilliferus” (Cros et al., 2000; Geisen et al., 2002);
Syracosphaera amoena with the former “Zygosphaerabannockii” and Corisphaera type A (Cros et al., 2000), andnow also with “Zygosphaera amoena” (Dimiza et al., inpress); Syracosphaera pulchra with the former “Calyptrosphaera oblonga” (Cros et al., 2000; Geisen et al., 2002)
and the former “Daktylethra pirus” (Geisen et al., 2002;
Saugestad & Heimdal, 2002); and Coronosphaera mediterranea with the former “Calyptrolithina wettsteinii”(Kamptner, 1941; Cros et al., 2000), “Calyptrolithophora2Malinverno, Triantaphyllou, Dimiza, Younghasleana” (Cortés & Bollmann, 2002) and “Zygosphaera
hellenica” (Geisen et al., 2002). Different mechanisms
have been proposed to explain these multiple combinations, involving non-genotypic variation in the degree ofcalcification in the holococcolith types (Cros et al., 2000,
for H. carteri), intraspecific variation, sexual dimorphism,hybridisation of two haploid phases, complex life-cycles,
and cryptic speciation, visible in the holococcolith phase,but not in the heterococcolith phase (Geisen et al., 2002,
for S. pulchra and C. mediterranea).
In this paper, we document two new possible heteroholococcolithophore combinations within the genus Syracosphaera: S. histrica with S. pulchra HOL oblonga typeand S. molischii with Gliscolithus amitakareniae. Additionally, we provide evidence of an ambiguous combination coccosphere, involving the two holococcolith forms of
S. pulchra, that is, HOL oblonga and HOL pirus. These
new combinations have the potential to add to the complexity of coccolithophore life-cycles known to date, involving multiple hetero-holococcolithophore combinations.
2. Material and methods
2.1 Sampling and observations
Water-samples, from which the two new possible heteroholococcolithophore combinations were observed, werecollected at 5m and 25m from Station N03 in the Ionian
Sea (eastern Mediterranean; Figure 1) during cruise SIN97
of the R/V Urania in December, 1997. Samples were obtained via Niskin bottles mounted on a rosette and controlled by a Seabird 911plus conductivitytemperature-depth (CTD) probe. Water-samples, containing further examples of previously described combinationsof Syracosphaera pulchra life-cycles, were collected from
Stations T3-5 and T1-100, at 45m (April, 2002) and 15m(September, 2004) depth, respectively, off Andros Islandin the Aegean Sea (Figure 1), using a single oceanographic
Hydro-bios bottle.

For all water-samples, 1.5 to 4l of sea-water were filtered through Millipore cellulose nitrate or cellulose acetate filters (0.45 to 0.8μm pore-size) using a vacuum
filtration system; for the coastal samples (off Andros), salt
was removed by washing the filters with about 2ml of bottled drinking water. The filters were oven dried and stored
in plastic Petri dishes.
Coccolithophores were subsequently identified andcounted by either light (LM) or scanning electron microscope (SEM). Their abundances and assemblage compositions in the pelagic Ionian and coastal Aegean Seas aredescribed, respectively, in Malinverno et al. (2003) andDimiza et al. (in press).
Two specimens, involving a combination of S. pulchra
HOL pirus type and S. pulchra HOL oblonga type holococcoliths, were found in separate sediment-trap samples,collected at 697m (Station 53) and 995m (Station 48)
depth, south of Crete Island (Figure 1). Samples were collected using PPS3/3 Technicap sediment-traps (0.125m2
collecting area), deployed from June, 2005 to May, 2006.
The sampling intervals are September, 2005 (53-IB8) andJanuary, 2006 (48-IIB5). Upon recovery, each sample wassplit into equal fractions using a rotary splitter (deviation
between aliquots 4%); one fraction was subsequently
treated for the analysis of coccolithophore fluxes, following the standard preparation techniques for sediment-trapsamples (e.g. see Broerse, 2000); total coccospheres, coccoliths and calcareous dinoflagellates were identified andcounted with the LM at 1250x magification. The total coccolithophore flux and assemblage composition at the different sites is described in Malinverno et al. (2007).
2.2 Terminology
For coccolithophore species identification, the classification scheme of Jordan et al. (2004) is followed. Following
the recommendations of Cros et al. (2000) and Young etal. (2003), well-established associations of hetero- andholococcolithophores are synonymised, and each phase isdefined informally by its hetero- (HET) or holococcolith (HOL) type and by its former specificname (e.g. Syracosphaera pulchra HOL oblongatype). When used, former species names are reported in double quotes (e.g. “Calyptrosphaera
oblonga”).

Figure 1: Sampling site locations in the eastern Mediterranean Sea. Water-sample
N03 from the Ionian Sea, sediment-trap samples 48 and 53 from south of Crete andwater-samples T3-5 and T1-100 from the Aegean Sea off Andros Island

3. Results and discussion
3.1 Syracosphaera histrica with S.
pulchra HOL oblonga type
A possible combination coccosphere (Pl.1, fig.1)
of Syracosphaera histrica (heterococcolithophore) and “Calyptrosphaera oblonga” (holococcolithophore) was recovered from Station N03
at 5m water-depth. This coccosphere is collapsed
and most coccoliths are in random orientations.
However, it contains no coccoliths from otherspecies and presents both ordinary and apical (defined by a little protrusion) holococcoliths from S.

Hetero-holococcolithophore combinations...Syracosphaera

3

Plate 1
SEM images of simple and combination coccospheres

5μm
Possible combination coccosphere of S. histrica endothecal (a) and exothecal (b) coccoliths with S. pulchra HOL oblonga type body (c) and apical (d) coccoliths (N03, 5m)

5μm
Simple heterococcosphere of S. histrica (N03, 10m)

5μm
5μm
Combination coccosphere of S. pulchra HET (a) and S. pulchra HOL pirus type(b) (T3-5, 45m)

Combination coccosphere of S. pulchra HET (a) and S. pulchra HOL oblonga
type (b) (T1-100, 15m)

10μm

10μm
Single holococcosphere of S. pulchra HOL pirus type (N11, 10m)

Simple holococcosphere of S. pulchra HOL oblonga type (N03, 10m)

2μm

5μm

Possible combination coccosphere of S. molischii type 3 (formerly S. corrugis)(a) and Gliscolithus amitakareniae (b) (N03, 25m)

Collapsed holococcosphere of G. amitakareniae (N03, 5m)

4Malinverno, Triantaphyllou, Dimiza, Young

3.2 Syracosphaera pulchra HOL oblonga
type with S. pulchra HOL pirus type
Two possible combination coccospheres of Syracosphaera
pulchra HOL pirus type and S. pulchra HOL oblonga type(Pl.2, figs 2, 3) were observed by LM in two sediment-trapsamples (53-IB8 and 48-IIB5) off Crete. In these two samples, “C. oblonga” coccospheres contributed 1.12% and6.29%, respectively, to the total coccosphere flux, while no“Daktylethra pirus” coccospheres were observed (thisspecies was, however, recovered in the samples as loose
coccoliths, although with approximately only half the percent abundance of “C. oblonga”, that is, 0.5% and 0.9%, respectively). This association is an ambiguous combination,
as the coccosphere shape is not regular, it has been documented only by LM, and was recovered from sediment-trapsamples, where the possibility of xenosphere formation ishigher. Nonetheless, it should be considered as a possibility, as it has been observed in two specimens. In this case,such evidence would suggest that either the two holococcolith types are directly related and represent a simple caseof intraspecific variation (although very rarely occurring inassociation), or that the association coccospheres are due tohybridisation, which could be possible, based on the genetic closeness of the two species.
Recent evidence has also shown a rather unambiguous
combination coccosphere of S. pulchra HOL pirus typewith S. protrudens (Triantaphyllou et al., in press), which
implies that S. pulchra and S. protrudens should be considered to be closely related (Figure 2). Previous LM observation by Kamptner (1941) recorded (but with noillustration) S. histrica in two different combinations with
Calyptrosphaera quadridentata (= Sphaerocalyptra
quadridentata) and with Calyptrosphaera gracillima (=Calyptrolithophora gracillima), while Cros et al. (2000,
pl.8, fig.2) showed an SEM image of a possible combination coccosphere of S. histrica and Calyptrolithophora papillifera.
“S. quadridentata” is now considered tobe the holococcolithophore phase of Algyrosphaera robusta, as they have both been reported to occur in several unambiguous
combination coccospheres (Kamptner, 1941;
Triantaphyllou & Dimiza, 2003; Malinverno
et al., in press). A more uncertain combination
with Rhabdosphaera clavigera has been documented by Cros & Fortuño (2002).
Although morphological similarity is not
a proven measure of taxonomic closeness, observations show that “S. quadridentata” and“C. oblonga” body coccoliths are relatively
alike, as they are built of microcrystals
arranged in a similar hexagonal mesh, although the former species displays a more irregular perforate pattern and has slightly
smaller and more distinctly conical coccoliths.
On the other hand, morphological observaFigure 2: Well-established (solid line) and possible (dashed line) syracosphaerid HETtions underline a close similarity between “C.
HOL combinations

pulchra HOL oblonga and both endo- and exothecal coccoliths from S. histrica. The specimen could represent a
chance collision of two coccospheres at some stage in thesediment-trap sampling process, or a faecal pellet containing two coccospheres, or a real combination coccosphere.
From this single specimen, a definitive conclusion cannot
be reached.
If we assume this is an authentic combination, however,
we face the problem of complex evolution or complex(multiple) life-cycles in Syracosphaera. In fact “C. oblonga” is now established as the holococcolithophore phaseof the life-cycle of S. pulchra (Pl.1, fig.4; Figure 2), and it
was thus transferred to this species as S. pulchra HOL oblonga type (Young et al., 2003). However, morphologicalobservations demonstrate strong affinities between S. pulchra and S. histrica, so that Young et al. (2003) and Geisen
et al. (2004) inferred they should be genetically close. S.
pulchra is also found in association with “Daktylethra
pirus” (Pl.1, fig.3; previously documented by SEM in
Geisen et al., 2002; LM evidence in Lecal-Schlauder, 1961;
Saugestad, 1967; Saugestad & Heimdal, 2002), which wasthus transferred to this species as S. pulchra HOL pirus
type (Geisen et al., 2002; Young et al., 2003). Among thevarious hypotheses to account for such complex associations, Geisen et al. (2002) proposed two likely alternative
explanations: cryptic speciation, that is, evolution withmorphological differentiation occurring only in the holococcolithophore phase and not evident in the heterococcolithophore phase, or complex life-cycles, involving
multiple hetero-holococcolithophore combinations. A third
possible hypothesis, that this was a case of intraspecificvariation within the holococcolithophore phase, was discarded on the grounds that the two holococcolithophore
forms have never been found co-occurring on the same
coccosphere, and intermediates between them do not occur.

Hetero-holococcolithophore combinations...Syracosphaera

5

Plate 2
LM images of established and possible combination coccospheres

5μm

LM image of a combination coccosphere of Syracosphaera pulchra HET and S. pulchra HOL oblonga type (Station T1-100, 15m)

low focus

high focus

5μm

LM images of a possible combination coccosphere of S. pulchra HOL oblonga type and S. pulchra HOL pirus type (same specimen, Station 48-IIB5)

oblonga” and C. papillifera. Ordinary calyptroliths have
similar hexagonal mesh construction and overall shape. In
the former species, however, they are slightly larger andpossess a convex distal surface, while in the latter, they
have flat distal surfaces bordered by a ring of crystallites.
Additionally, a basal ring, one crystallite thick, is present in

C. papillifera, but more developed in “C. oblonga”. Apicalcoccoliths of “C. oblonga” are slightly more elevated thanordinary ones, and have a distal, pointed, pyramidal spine;in C. papillifera, they are highly vaulted, with flat sides andan elevated central-area with parallel strings of crystals.
They show well-separated morphological characteristics,

6

Malinverno, Triantaphyllou, Dimiza, Youngand thus seem to be distinct species. However, several
specimens have coccoliths with mixed characters (MD &MVT, pers. obs., 2007), suggesting these could be a new
Calyptrolithophora species. If substantiated by further observations, the newly-discovered combination coccosphere
found in our samples would imply a complex relationshipbetween three heterococcolithophore types linked withthree holococcolithophore types, in combinations of oneto-one or one-to-two (Figure 2). Intriguingly, it is still possible to resolve the rather confusing set of potential
associations into a single coherent evolutionary scheme(Figure 3). The evidence for this scheme is weak, but it
does highlight the possibility that uncoupled evolution of
the haploid and diploid phases may make life-cycle associations of coccolithophore types excellent indicators ofphylogenetic relationships.

with no clear separation of the diagnostic characters; type
2 of Young et al. (2003) corresponds to S. elatensis Winterin Winter et al., 1979, while type 3 corresponds to S. corrugis Okada & McIntyre, 1977. The combination coccosphere shown by Cros & Fortuño (2002) includes S.
molischii type 2, with teeth protruding from the inner partof the coccolith’s distal flange towards the central-area, anda strongly-calcified central-area structure. In contrast, thecoccosphere of our sample includes S. molischii type 3, in
which coccoliths have no teeth protruding towards the central-area and a less-calcified central-area structure.
None of the two S. molischii coccospheres found up to
now in combination with holococcoliths represents an unambiguous association. However, if these combinations
eventually prove to be real, they would strengthen the argument for separation of S. molischii types into separate
species.

4. Conclusions
Here we have demonstrated two new examplesof possible combination coccospheres, Syracosphaera histrica with S. pulchra HOL oblonga type and S. molischii with Gliscolithus
amitakareniae. Additionally, we have documented an ambiguous specimen, showing coccoliths of both S. pulchra HOL oblonga typeand S. pulchra HOL pirus type. Although all
specimens are represented by equivocal combinations, which are not confirmed by multiple
examples, they potentially document new lifecycle associations within coccolithophores. If
confirmed, these new combinations would
imply that the relationships between different
phases, at least within the genus Syracosphaera,
are more complex than explained to date, andthey may provide invaluable phylogenetic data.
Figure 3: Possible evolutionary scheme for the Syracosphaera pulchra-S. histrica-S.
Clearly,
there is a need for more observations ofprotrudens plexus, involving independent evolution of the HET and HOL phasescombination coccospheres, and other lines of
3.3 Syracosphaera molischii withevidence, in order to elucidate coccolithophore life-cycles,
Gliscolithus amitakareniae
and realise their potential as indicators of evolutionary reA single heterococcosphere of Syracosphaera molischii, in lationships and keys to understanding coccolithophore
which is embedded a single holococcolith of Gliscolithus ecology.
amitakareniae, was recovered from Station N03 at 25m
water-depth (Pl.1, fig.7). This specimen does not represent Acknowledgements
an unambiguous combination, as only one coccolith of G. Financial support for collection and study of samples from theamitakareniae is present. It is, however, unlikely that this Ionian Sea, Aegean Sea and offshore Crete was provided, respecimen represents a xenosphere, as the holococcolith ap- spectively, by the Italian Project SINAPSI (Seasonal, INterannualand decAdal variability of the atmosPhere, oceanS and related
pears embedded within the heterococcolith coccosphere.
marIne ecosystems), 01ED100/PENED Project andPreviously, Cros & Fortuño (2002, fig.112A) docu04EP59/ENTER Project of the European Union and the Generalmented a possible combination coccosphere of S. molischii Secretariat for Research and Technology/Greek Ministry of Deand Anthosphaera fragaria. The specimen, however, was velopment. This work was carried out within research project
collapsed and could, therefore, be simply a chance associ- ENTER, co-financed by EU-European Social Fund (75%) and theation. Different types of S. molischii have been informally Greek Ministry of Development - GSRT (25%). Dr. Markus
distinguished by Young et al. (2003), based on the orna- Geisen and Dr. Lluïsa Cros are warmly acknowledged for careful
mentation of the distal flange and of the central-area. The review of the manuscript and for suggestions to its improvement.
S. molischii species concept includes, in fact, morphologies that were formerly described independently, althoughHetero-holococcolithophore combinations...Syracosphaera

References
Alcober, J. & Jordan, R.W. 1997. An interesting association between Neosphaera coccolithomorpha and Ceratolithus cristatus (Haptophyta). European Journal of Phycology, 32: 91-93.
Broerse, A.T.C. 2000. Coccolithophore export production in selected ocean environments: seasonality, biogeography, carbonate production. Unpublished PhD thesis, Vrije
Universiteit, Amsterdam.
Cortés, M.Y. 2000. Further evidence for the heterococcolith-holococcolith combination Calcidiscus leptoporus-Crystallolithus
rigidus. Marine Micropaleontology, 39: 35-37.
Cortés, M.Y. & Bollman, J. 2002. A new combination coccosphere of the heterococcolith species Coronosphaera mediterranea and the holococcolith species Calyptrolithophora
hasleana. European Journal of Phycology, 37: 145-146.
Cros, L. & Fortuño, J.-M. 2002. Atlas of Northwstern Mediterranean coccolithophores. Scientia Marina, 66 (supplement 1):
1-186.
Cros, L., Kleijne, A., Zeltner, A., Billard, C. & Young, J.R. 2000.
New examples of holococcolith-heterococcolith combination
coccospheres and their implications for coccolithophorid biology. Marine Micropaleontology, 39: 1-34.
Dimiza, M.D., Triantaphyllou, M.V. & Dermitzakis, M.D. In
press. Seasonality and ecology of living coccolithophores in
E. Mediterranean coastal environments (Andros Island, Middle Aegean Sea). Micropaleontology.
Geisen, M., Billard C., Broerse, A.T.C., Cros, L., Probert, I. &Young, J.R. 2002. Life-cycle associations involving pairs of
holococcolithophorid species: intraspecific variation or cryptic speciation? European Journal of Phycology, 37: 531-550.
Geisen, M., Young, J.R., Probert, I., Saez, A., Baumann, K.-H.,
Bollmann, J., Cros, L., de Vargas, C., Medlin, L. & Sprengel,
C. 2004. Species level variation in coccolithophores. In: H.
Thierstein & J.R. Young (Eds). Coccolithophores: From Molecular Processes to Global Impact. Springer, Berlin: 327366.
Houdan, A., Billard, C., Marie, D., Not, F., Sàez, A.G., Young,
J.R. & Probert, I. 2004. Flow cytometric analysis of relative
ploidy levels in holococcolithophore heterococcolithophore(Haptophyta) life cycles. Systematics and Biodiversity, 1:
453-465.
Jordan, R.W., Cros, L. & Young, J.R. 2004. A revised classification scheme for living haptophytes. In: M.V. Triantaphyllou(Ed.). Advances in Biology, Ecology and Taphonomy of Extant Calcareous Nannoplankton. Micropaleontology, 50, supplement 1: 55-80.
Kamptner, E. 1941. Die Coccolithineen der Südwestküste vonIstrien. Annalen des Naturhistorischen Museums in Wien, 51:
54-149.
Kleijne, A. 1991. Holococcolithophorids from the Indian Ocean,
Red Sea, Mediterranean Sea and North Atlantic Ocean. Marine Micropaleontology, 17: 1-76.
Lecal-Schlauder, J. 1961. Anomalies dans la composition des coques de flagellés calcaires. Bulletin de la Société d’Histoire
Naturelle de l’Afrique du Nord, 52: 63-66.
Malinverno, E., Dimiza, M.D., Triantaphyllou, M.V., Dermitzakis, M.D., Corselli, C. In press. Coccolithophores of the eastern Mediterranean Sea: a look into the marine micro world. (Icoccolitoforidi del Mar Mediterraneo orientale: uno sguardo
nel microcosmo marino.) ION Publications, Athens: 180pp.
Malinverno, E., Triantaphyllou, M., Stavrakakis, S., Ziveri, P.,
Lykousis, V. 2007. Coccolithophore export production andflux at the south-western margin of Crete (Eastern Mediter-

7

ranean). Geophysical Research Abstracts, 9: 16077962/gra/EGU2007-A-08093.
Malinverno, E., Ziveri, P. & Corselli, C. 2003. Coccolithophorid
distribution in the Ionian Sea and its relationship to eastern
Mediterranean circulation during late fall to early winter1997. Journal of Geophysical Research, 108(C9), No.C9,
8115, doi:10.1029/2002JC001346.
Manton, I. & Leedale, G.F. 1969. Observations on the microanatomy of Coccolithus pelagicus and Cricosphaera
carterae with special reference to the origin and nature of coccoliths and scales. Journal of Marine Biology Association,
UK, 49: 1-16.
Noël, M-H., Kawachi, M. & Inouye, I. 2004. Induced dimorphic
life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea(Prymnesiophyceae, Haptophyta). Journal of Phycology, 40:
112-129.
Okada, H. & Mcintyre, A. 1977. Modern coccolithophores of the
Pacific and North Atlantic Oceans. Micropaleontology, 23: 155.
Parke, M. & Adams, I. 1960. The motile (Crystallolithus hyalinus
Gaarder and Markali) and non-motile phases in the life historyof Coccolithus pelagicus Schiller. Journal of the Marine Biological Association of the United Kingdom, 39: 263-274.
Rowson, J.D., Leadbeater, B.S.C. & Green, J.C. 1986. Calcium
carbonate deposition in the motile Crystallolithus phase of
Coccolithus pelagicus (Prymnesiophyceae). British Phycological Journal, 21: 359-370.
Samtleben, C. & Scröder, A. 1992. Living coccolithophore communities in the Norwegian-Greenland Sea and their record insediments. Marine Micropaleontology, 19: 333-354.
Saugestad, A.H. 1967. Planteplankton i vestlige Middlehav marsapril 1961. Unpublished MSc thesis, University of Oslo:
124pp. [In Norwegian]
Saugestad, A.H. & Heimdal, B.R. 2002. Light microscope studies on coccolithophorids from the western Mediterranean Sea,
with notes on combination cells of Daktylethra pirus andSyracosphaera pulchra. Plant Biosystems, 136: 3-28.
Thomsen, H.A., Østergaard, J.B. & Hansen, L.E. 1991. Heteromorphic life histories in arctic coccolithophorids (Prymnesiophyceae). Journal of Phycology, 27: 634-642.
Triantaphyllou, M.V. & Dimiza, M.D. 2003. Verification of the
Algirosphaera robusta – Sphaerocalyptra quadridentata (coccolithophores) life-cycle association. Journal of Micropalaeontology, 22: 107-111.
Triantaphyllou, M.V., Dimiza, M.D. & Dermitzakis, M.D. 2004.
Syracosphaera halldalii - Calyptolithina divergens var.
tuberosa life-cycle association and relevant taxonomic remarks. In: M.V. Triantaphyllou (Ed.). Advances in Biology,
Ecology and Taphonomy of Extant Calcareous Nannoplankton. Micropaleontology, 50, supplement 1: 121-126.
Triantaphyllou, M.V., Dimiza, M.D., Malinverno, E. & Young,
J.R. In press. Evidence for a possible life-cycle association
between Syracosphaera protrudens (heterococcolithophore)and Syracosphaera pulchra HOL pirus-type (holococcolithophore). Journal of Micropalaeontology.
Winter, A., Reiss, Z. & Luz, B. 1979. Distribution of Living Coccolithophore Assemblages in the Gulf of Elat (‘AQABA).
Marine Micropaleontology, 4: 197-223.
Winter, A. & Siesser, W.G. 1994. Atlas of living coccolithophores.
In: A. Winter & W.G. Siesser (Eds). Coccolithophores. Cambridge University Press, Cambridge: 107-159.
Young, J.R., Bergen, J.A., Bown, P.R., Burnett, J.A., Fiorentino,A., Jordan, R.W., Kleijne, A., Niel, B.E. van, Romein, A.J.T.

8Malinverno, Triantaphyllou, Dimiza, Young& von Salis, K. 1997. Guidelines for coccoliths and calcareous nannofossil terminology. Palaeontology, 40: 875-912.
Young, J.R. & Geisen, M. 2002. Xenospheres – associations ofcoccoliths resembling coccospheres. Journal of Nannoplankton Research, 24(1): 27-35.
Young, J.R., Geisen, M., Cros, L., Kleijne, A., Sprengel, C.,
Probert, I. & Østergaard, J. 2003. A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research,Special Issue 1: 1-125.
Young, J.R., Jordan, R.W. & Cros, L. 1998. Notes on nannoplankton systematics and life-cycles. Ceratolithus cristatus,
Neosphaera coccolithomorpha and Umbilicosphaera sibogae. Journal of Nannoplankton Research, 20(2): 89-99.