J. Nannoplankton Res. 31 (2), 2010, pp.114-120 © 2010 International Nannoplankton Association, Inc.
ISSN 1210-8049 Printed by The Sheridan Press, Hanover, PA, USA114

Possible affinities between the holococcolithophores
Syracosphaera pulchra HOL oblonga-type andCalyptrolithophora papillifera
Maria V. Triantaphyllou
Department of Historical Geology & Palaeontology, University of Athens, Panepistimiopolis 15784, Athens, Greece; mtriant@geol.uoa.gr

Manuscript received 20th July, 2009; revised manuscript accepted 13th May, 2010

Abstract Several coccospheres, composed of typical Syracosphaera pulchra HOL oblonga-type body and apicalcoccoliths and a varying number of flat-topped coccoliths that resemble Calyptrolithophora papillifera, have been observed in samples from the Aegean Sea. The observed coccospheres indicate that the morphology of these two holococcolithophores may be less distinct than has been previously assumed.
Keywords Living coccolithophores, life-cycle, holococcoliths
1. Introduction
Coccolithophores, the most productive calcifying organisms on Earth, have been shown, from a number of culture
studies, to have life-cycles typically involving alternation
between a haploid holococcolith-producing phase and adiploid heterococcolith-producing phase (e.g. Parke &Adams, 1960; Houdan et al., 2004). A significant numberof field studies have revealed the existence of spectacular
combination coccospheres that represent the moment oflife-cycle transition (Kamptner, 1941; Lecal-Schlauder,
1961; Kleijne, 1991; Thomsen, 1991; Alcober & Jordan,
1997; Young et al., 1998; Cros et al., 2000; Cortes, 2000;
Cortes & Bollmann, 2002; Geisen et al., 2002; Cros & Fortuño, 2002; Triantaphyllou & Dimiza, 2003; Triantaphyllou
et al., 2004, 2009; Geisen et al., 2004; Malinverno et al.,2008a; Frada et al., 2009). In many cases, a single holococcolith type is associated with a single heterococcolith
type. In several other cases, however, one heterococcolith
is associated with two or more holococcolith types. These
more complex associations have been inferred to indicate
either intraspecific varation in holococcolith morphology(e.g. Helicosphaera carteri) or sets of sibling species, inwhich the discrete species can only be distinguished in theholococcolith stage (e.g. Syracosphaera pulchra: Cros etal., 2000; Geisen et al., 2002; Saugestad & Heimdal, 2002;
Malinverno et al., 2008a; Dimiza et al., 2008; Triantaphyllou et al., 2009).
The main objective of the present study is to further our
understanding of coccolithophore life-cycles by describing
an unusual holococcolith morphotype that seems to havecharacteristics in common with both Calyptrolithophora
papillifera and Syracosphaera pulchra HOL oblonga-type(the former Calyptrosphaera oblonga).
2. Material and methods
In total, 13 water samples were analysed during the present
study. Five samples were collected on April 18th, 2006
from three stations in the Evoikos Gulf (western continental shelf of the Aegean Sea), using a single oceanographic

Hydro-bios bottle. In addition, eight samples were collected on February 2nd, 2007 from one station in the Skyros Basin (northern Aegean Sea) during the Meteor M71-3
cruise (Emeis, 2007). The locations of the samples, waterdepth, temperature and salinity data are presented in Figure
1 and Table 1.

Figure 1: Location of the sampled stations in the Aegean Sea. Water samples Ev-2, Ev-3, Ev-4 from Evoikos Gulf, Sk-1 from northern Skyros
Basin

For each sampling depth, 2l of sea-water was filteredthrough a Whatman cellulose nitrate filter (47mm diameter,
0.45μm pore-size), using a vacuum filtration system. Salt
was removed by washing the filters with about 2ml of mineral water. The filters were oven dried and stored in plastic
Petri dishes. A piece of each filter, approximately 8 x

115

Triantaphyllou

8mm2, was attached to a copper electron microscope stubusing double-sided adhesive tape, and coated with gold.
The filters were examined in a Jeol JSM 6360 ScanningElectron Microscope (SEM) and all the individual coccolithophore specimens occurring on the examined filter piece
were identified and counted. A working magnification ofx1200 was used throughout the counting.

cells/l) and Calyptrolithina wettsteinii (up to 1.2x103
cells/l).
In the winter coccolithophore assemblages from thenorthern Skyros Basin, 20 heterococcolithophore and only
two holococcolithophore species were present (Table 2).
The total cell density ranged from 1.3x103 to 31.4x103
cells/l, whereas species richness ranged between two and11 species. E. huxleyi was the dominant species (up to
15.8x103 cells/l). Rhabdosphaera clavigera
Station Date Latitude Longitude Water depth Temperature Salinity
preferred the upper photic zone (up to 3.1x103
(m)
(˚C)
(psu)
cells/l), whereas in the lower photic zone, AlEv- 2 18/4/06 38˚09.32'N 24˚03.00'E
5
15.40
37.00
girosphaera robusta became a significant
Ev- 3
38˚06.28'N 24˚00.70'E
5
14.80
37.00
component of the nannoflora (up to 1.3x103
15
14.70
37.00
cells/l). Holococcolithophores were repreEv- 4
38˚07.08'N 24˚02.49'E
5
15.30
37.00
sented only by S. pulchra HOL oblonga-type
15
14.90
37.10
and C. wettsteinii. In general, they were pres30
14.70
37.10
ent in few samples and occurred in low abundances (<0.5x103 cells/l).
Sk-1 2/2/07 39˚33.36'N 23˚48.00'E
5
13.65
38.12
Calyptrolithophora papillifera was
20
13.66
38.12
found in the spring assemblages of the Evoikos
43
14.84
38.66
50
15.00
38.75
Gulf, only at 5m water-depth. In contrast, S.
80
14.93
38.91
pulchra HOL oblonga-type was relatively very
100
14.67
38.89
abundant throughout the upper 30m of the
200
14.09
38.89
water-column in the spring assemblages,
whereas it was found only at 20m water-depth
Table 1: Locations of the studied samples and environmental parametersin the winter assemblages of the northern Skyros Basin.
Coccolithophore cell density (number of cells/l) was
Thirty-four coccospheres were observed in the Evoikos
calculated following the methodology of Jordan & Winter samples, and an additional one in the Skyros samples, bear(2000), by scaling up the raw counts from a known scanned ing coccoliths which have characteristics somewhat inarea, using the equation,common with C. papillifera and S. pulchra HOL oblongatype (Plates 1, 2). In detail, the observed coccospheres feaA = N x S/Vture ‘C. oblonga’ body and apical coccoliths and also avarying number of flat-topped coccoliths that look like C.
where N is the number of cells of a species on the whole papillifera.
piece of filter, S the scaling factor (area of the whole filter/area of scanned filter piece), V the volume of the sea- 4. Discussion and conclusions
water filtered (in l), and A the absolute abundance of the Syracosphaera pulchra HOL oblonga-type (‘C. oblonga’)
species in cells/l. All the filter samples and the SEM mi- and Calyptrolithophora papillifera have body coccoliths
crographs are kept in the collections of the Museum of of similar shape and size, which show hexagonal-mesh
Palaeontology & Geology at the University of Athens.
wall-fabrics. They are, however, usually clearly separated
by a number of differences. Coccospheres of ‘C. oblonga’
3. Results
have spherical to subspherical shape, with >100 elliptical,
The observed spring coccolithophore assemblages from cap-shaped calyptroliths, formed by hexagonal crystallites.
Evoikos Gulf comprise 14 heterococcolithophore and nine A proximal ring with three to four rows of crystallites, one
holococcolithophore species (Table 2). The total cell den- crystallite thick, forms a basal flange. The apical coccolsity varied between 6.4x103 and 11.7x103 cells/l. The high- iths are similar, with a well developed pyramidal spine exest species richness (13 taxa) was observed at Stations tending distally (Young et al., 2003; Malinverno et al.,Evoikos-2 at 5m and Evoikos-4 at 30m, and the lowest 2008b).
(eight taxa) at Station Evoikos-4 at 5m. Emiliania huxleyi
C. papillifera has a dimorphic, spherical to elongated
was the major heterococcolithophore component of the coccosphere made of 100-150 coccoliths. The body coccommunities (up to 5.2x103 cells/l), followed by Syra- coliths are elliptical, built of hexagonal crystallites. The
cosphaera pulchra (up to 2.8x103 cells/l) and Syra- tube is eight to nine crystallites high, one crystallite wide,
cells/l). with a single-crystallite-wide basal flange. The distal surcosphaera
nodosa(up
to
0.8x103
Holococcolithophores showed relatively high absolute face is flat, with a perforated hexagonal mesh and no larger
abundances (up to 5.7x103 cells/l), being represented perforations. Apical coccoliths are highly vaulted, with flat
mostly by S. pulchra HOL oblonga-type (up to 4.2x103 sides and a central elevated area and with parallel strings ofPossible affinities between holococcolithophores

89

179

4196

Zygosphaera hellenica

S. pulchra HOL pirus type

2248

Table 2: Species cell densities (cells/l) in the studied samples

3564
64
Homozygosphaera arethusae

83

83

83
128

C. wettsteinii
Helicosphaera carteri HOL

96

2248

96

2312

446

S. pulchra HOL oblonga type

674

289
64

642
1156
578
128

1028

Calyptrolithophora papillifera

96

96

96

96
83
Umbellosphaera tenuis
Calcidiscus quadriperforatus HOL

Syracosphaera sp.

H. vercellii
Syracosphaera anthos HOL

803

64

64
89

625
2216
289
2808
385

S. pulchra
Syracosphaera sp. type L

2184

289
193
64
S. protrudens

128

193

193

193

385

193

257
96
128
83
64
S. ossa

165
S. molischii

S. lamina

S. histrica

96

89

482
771
661
193

96
193
Syracosphaera corolla

64
Rhabdosphaera clavigera

Ophiaster hydroideus

Gladiolithus flabellatus

Gephyrocapsa oceanica

Florisphaera profunda

S. nodosa

450

2762
3179
3468
1798
Emiliania huxleyi

Cyrtosphaera lecaliae

Calciosolenia murrayi
Canistrolithus sp.1 POL

Alisphaera gaudii

Algirosphaera robusta

268

64

128

771

193

3083
64

1220

cosphere with the heterococcolithophore Syracosphaera
protrudens (Triantaphyllou et al., 2009). This rather confusing coccolithophore suite has been further added to byobservations of a collapsed possible-combination coccosphere of Syracosphaera histrica with C. papillifera (Croset al., 2000), and possible combinations between S. pulchra HOL oblonga-type and S. pulchra HOL pirus-type,and also of S. histrica with S. pulchra HOL oblonga-type(Malinverno et al., 2008a).
The documented specimens of the present study havecoccoliths with mixed characteristics, seemingly intermediate between ‘C. oblonga’ and C. papillifera (e.g. Plates 1,2), however the numerous flat-topped coccoliths observedin the coccospheres do not really look like C. papillifera
as, when seen in side view, they have well-developed basal
flanges (Pl.2, fig.3), typical of ‘C. oblonga’ (Pl.1, fig.1),
but not of C. papillifera (Pl.1, fig.2), and there is no obvi-

5106

268

89

193

15799
10597

128
89

5178

193
64
64
A. quattrospina

Acanthoica acanthifera

110

21389
12650
12408
11752
8606
8095
6421
Total standing crop (cells/l)

9632

Sk-1 5

199
139

Ev-4 30
Ev-4 15121
134

Ev-4 598
100

Ev-3 15
Ev-3 5Ev-2 5
Stations

Number of specimens/sample

100Sk-1 20

crystallites (Young et al., 2003; Malinverno et al., 2008b).
Comparison between ‘C. oblonga’ and C. papillifera reveals that ordinary calyptroliths in the former species areslightly higher and possess a convex distal surface, while in
the latter they have a flat distal surface. Additionally, thebasal ring is present in C. papillifera, but more developedin ‘C. oblonga’, and the apical coccoliths of ‘C. oblonga’show characteristics well-separated from those of C. papillifera.
Both holococcolithophore types have been shown toform combination coccospheres with heterococcoliths. In
particular, ‘C. oblonga’ has been found with S. pulchra(Lohmann, 1902; Kamptner, 1941; Cros et al., 2000;
Geisen et al., 2002), which also forms combinations with
S. pulchra HOL pirus-type (the former Daktylethra pirus:
Geisen et al., 2002; Saugestad & Heimdal, 2002). ‘D.
pirus’ has also been observed forming a combination coc-

116

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Triantaphyllou

Plate 1

Coccosphere of S. pulchra HOL oblonga-typeEv-2, 5m

Coccosphere of C. papillifera
Ev-2, 5m

Coccosphere of C. papillifera-like coccoliths/flat-topped S. pulchra HOL oblonga-type body coccoliths (a) and S. pulchra HOL
oblonga-type body and apical coccoliths (b)Ev-2, 5m

Coccospheres of C. papillifera-like coccoliths/flat-topped S. pulchra HOL oblonga-type body coccoliths (a) and S. pulchra HOL
oblonga-type body and apical coccoliths (b)Ev-2, 5m

Possible affinities between holococcolithophores

118

Plate 2

Coccospheres of C. papillifera-like coccoliths/flat-topped S. pulchra HOL oblonga-type body coccoliths (a) and S. pulchra HOL
oblonga-type body and apical coccoliths (b)Ev-4, 5m

Coccospheres of C. papillifera-like coccoliths/flat-topped S. pulchra HOL oblonga-type body coccoliths (a) and S. pulchra HOL
oblonga-type body and apical coccoliths (b)Ev-4, 15m

C. papillifera-like coccoliths (a), S. pulchra HOL oblonga-typebody coccoliths (b) and S. pulchra HET (c)Sk-1, 20m

C. papillifera-like coccoliths (a), S. pulchra HOL oblonga-typebody coccoliths (b)Ev-4, 5m

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Triantaphyllou

ous sign of papillifera-type apical coccoliths (Pl.2, fig.6).
However, there are examples where a difference can beseen between ‘C. oblonga’ body and apical coccoliths andvery thin, almost transparent (Pl.2, fig.2), flat coccoliths
that resemble C. papillifera. An interesting example is presented in Plate 2, fig.5, where a coccosphere with C. papillifera-like coccoliths and S. pulchra HOL oblonga- typecoccoliths includes one body coccolith of S. pulchra HET.
It is possible that the observed C. papillifera-like/flattopped ‘C. oblonga’ body coccoliths may be malformed ordamaged specimens, or may even represent a variant of ‘C.
oblonga’ with slightly atypical morphology. However, although not being true combination coccospheres, the documented specimens may suggest a link between ‘C.
oblonga’ and C. papillifera that supports previous observations documenting combination coccospheres of both ‘C.
oblonga’ and C. papillifera with the same heterococcolithophore species, S. histrica (Cros et al., 2000; Malinverno
et al., 2008a). The suggested affinities between ‘C. oblonga’ and C. papillifera, in combination with the relationship proposed between ‘C. oblonga’ and ‘D. pirus’(Malinverno et al., 2008a), adds to the implications concerning the Syracosphaera pulchra-S. histrica-S. protrudens plexus being associated with three holococcolithore
types (‘D. pirus’, ‘C. oblonga’ and C. papillifera), as thesewere tentatively incorporated into a possible evolutionary
scheme (Malinverno et al., 2008a).
Acknowledgments
Financial support for this study was provided by Research Project 70/4/8644 of the University of Athens. Special thanks are due
to K.-C. Emeis and G. Anastasakis for providing part of the study
material. Jeremy Young and Lluïsa Cros are warmly acknowledged for constructive criticism and careful reviews of the manuscript.

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