&RFFROLWKRSKRUHV$EVWUDFWV37

New evidence for the ecology of Helicosphaera carteri
in polluted coastal environments (Elefsis Bay, Saronikos
Gulf, Greece)
Margarita D. Dimiza, Maria V. Triantaphyllou
Faculty of Geology & Geoenvironment, University of Athens, Greece; mdimiza@geol.uoa.gr; mtriant@geol.uoa.gr

Elisa Malinverno
Department of Earth and Environmental Sciences, University of Milano-Bicocca, Italy

Abstract: The Elefsis Bay is a typical coastal setting characterized by a semi-closed shallow environment withintense anthropogenic activity. This study describes a peculiar low cell density and species poor late-winter coccolithophore assemblages from Elefsis Bay compared to those from further offshore of the Aegean Sea. Helicosphaera carteri
FRQWULEXWHVVLJQLÀFDQWO\WRWKHDVVHPEODJHLQVLGHWKH(OHIVLV%D\DQGWRJHWKHUZLWKEmiliania huxleyiERWKUHSUHVHQWWKHGRPLQDQWFRPSRQHQWRIWKHFDOFDUHRXVQDQQRSODQNWRQ:DWHUFROXPQGDWDFRQÀUPHGWKHRSSRUWXQLVWLFEHKDYLRURI
H. carteri, thus providing new evidence for the ecology of the species. It is suggested that an increase in this species
can be associated with distinct pollution in neritic environments.
Keywords: living coccolithophores, eutrophication-polluted, Aegean, Ionian Seas
1. Introduction
The Aegean Sea has been described as one of the mostoligotrophic areas of the eastern Mediterranean, characterized by low biological production (e.g., Ignatiades,
1998; Psarra et al., 2000). However, an established N-S
trophic gradient exists from mesotrophic to ultra-oligotrophic regions. The northern Aegean Sea is relatively
PHVRWURSKLF EHLQJ LQÁXHQFHG E\ IUHVKZDWHU GLVFKDUJHV
from rivers and seasonally varying input of Black Sea
surface water through the Dardanelles Straits (Ignatiades et al., 2002; Zervoudaki et al., 2011; Lagaria et al.,2013). Additional areas such as the coastal Saronikos andEvoikos gulfs and the open-ocean Rhodes cyclonic gyredisplay similar trophic features. In contrast, the “typicaloceanic margin” of South Aegean Sea is an oligotrophic
to ultra-oligotrophic environment, with very low export
rates of organic carbon and organic-poor sediments (e.g.,
Gogou et al., 2000; Lykousis et al., 2002). In the northern
Aegean Sea, diatoms are the most abundant componentsof the phytoplankton (Lykousis et al., 2002), whereas in
the south Aegean Sea, coccolithophores are one of the

Figure 1. Bathymetric map of the study area and location of the stations sampled for coccolithophore analysis, $. Elefsis Bay, B. off-shore
Aegean environments.

major primary producers (Ignatiades et al. 2002; Triantaphyllou et al. 2004). Emiliania huxleyi dominates thewinter coccolithophore assemblages, followed in summer
by holococcolithophores and Rhabdosphaeraceae andSyracosphaera spp. (Dimiza et al., 2008 a,b).
Despite the oligotrophic nature of the South AegeanSea, eutrophication problems, indicated by elevatednutrient data, have been recognized locally in a number ofcoastal areas as a result of increased anthropogenic activities (e.g., Sklivagou et al., 2008; Pavlidou, 2012; Kapsimalis et al., 2014). One of the most impacted coastal areasof Greece is the shallow semi-closed Elefsis Bay, locatedat the northern edge of the Saronikos Gulf (Fig. 1). The
present study describes late-winter coccolithophore abundances and species composition in the restricted environment of Elefsis Bay, highlighting the opportunistic
behavior of Helicosphaera carteri in neritic environmentswith elevated pollutant inputs.
2. Materials and methods
Two water samples (5 and 20 m water depth) were collected

38&RFFROLWKRSKRUHV$EVWUDFWV

Stationsampling period

Water depth(m)

S2

February 2012

5, 20

M1

January 2011

3, 20

M2

January 2011

3, 20

M3

January 2011

2, 20

M4 (AMT7)January 2011

2, 10, 20

T1-3

March 2002

5, 15

T1-4

March 2002

5, 15

T1-5

March 2002

5, 10

T1-6

March 2002

5, 10

T1-8

March 2002

0, 5

HAS

February 2012

5, 30

Table 1. Sampling period and water depth from each sampled station.

Station

Water
depth
(m)

Total
coccospheredensity(x 103
cells/l)from station S2 in Elefsis Bay (38o00.00’, 23o27.24’;
Fig. 1A), during the R/V AEGAEO cruise (February
2012, FP7 Perseus Project). The Elefsis assemblages arecompared with winter and early spring coccolithophore
assemblages from several water samples in different environments, collected at depths between 0 and 30 m (Table1). The data set comes from 10 stations (Fig. 1B) in the
North Aegean (M1-4: Athos basin), central Aegean (T1:
Andros Island - 5 stations), and South Aegean Sea (HAS:
Antikythira straits).
For each sampling depth, 2 liters of seawater wereÀOWHUHGRQ:KDWPDQFHOOXORVHQLWUDWHÀOWHUV PPGLDPHWHUPPSRUHVL]H XVLQJDYDFXXPÀOWUDWLRQV\VWHP
6DOWZDVUHPRYHGE\ZDVKLQJWKHÀOWHUVZLWKDERXWPO
RIPLQHUDOZDWHU7KHÀOWHUVZHUHRSHQGULHGDQGVWRUHGLQSODVWLF3HWULGLVKHV$SLHFHRIHDFKÀOWHUDSSUR[LPDWHO\
8x8 mm2 was attached to a copper electron microscope
stub using a double-sided adhesive tape and coated with
JROG7KHÀOWHUZDVWKHQH[DPLQHGZLWKD-HRO-60

HeliSyraRhabEmiliania
cosphaera cosphaera dosphaerhuxleyi
spp.
aceae
carteri(x 102(x 102(x 102(x 102cells/l)cells/l)cells/l)cells/l)Gephyrocapsa
oceanica(x 102cells/l)Holococcolithophores(x 102cells/l)otherspecies(x 102cells/l)species
diversity(S)

ShannonWiener
index (H)

1.9

3

0.81

2.9

4

0.90

semi closed Elefsis Bay
S2

5

4.6

17

27.5

20

5.1

20

27.9

0.5

off-shore marine environments of the Aegean Sea
M1

M2

M3

M4

T1-3

T1-4

T1-5

T1-6

T1-8

HAS

3

29.5

270

16.1

9.0

0.6

20

22.0

200

13.5

5.1

0.6

0.50

11

0.48

6.4

15

0.69

3.2

18

0.63

3

19.3

161

14.1

9.6

20

25.9

228

19.3

8.3

2

33.7

331

33.3

1.7

1.3

0.5

22

0.76

20

34.9

298

37.9

7.7

2.6

2.6

18

0.68

2

27.7

249

20.5

5.8

0.6

0.6

17

0.53

10

37.5

354

8.3

10.9

20

33.9

318

15.4

3.2

0.6

2.6

16
0.6

0.6

0.6

14

0.34

1.9

13

0.37

5

35.3

326

17.3

2.6

1.3

4.5

12

0.39

15

19.8

191

1.9

0.6

0.6

4.5

7

0.22

5

27.9

270

5.8

0.6

0.6

0.0

2.6

8

0.20

15

25.8

244

9.0

1.9

1.3

0.0

1.3

9

0.30

0.6

0.0

1.3

8

0.23

1.3

2.6

8

0.23

5

13.7

132

3.2

10

27.6

265

7.1

5

20.2

193

7.7

10

21.8

213

0.6

0

9.2

87

5

11.4

105

5

18.4

132

30

19.6

155

0.6

0.6

0.6

7

0.25

0.6

0.6

1.9

8

0.14

0.6

0.6

1.9

8

0.35

0.6

1.9
7.7

0.6

0.6

7

0.40

2.6

13.5

14.8

3.8

17.3

26

1.42

24.4

7.1

3.8

26.1

24

1.07

Table 2. Total coccolithophore density, species diversity, Shannon–Wiener index and abundance of the most common coccolithophore taxa.

&RFFROLWKRSKRUHV$EVWUDFWVScanning Electron Microscope (University of Athens,
Department of Historical Geology and Palaeontology).
Coccolithophore densities (coccospheres/l) were calculated following the methodology of Jordan and Winter(2000).
Species diversity (S) and Shannon Shannon–Wiener
diversity index (H) were calculated using the Past software package vers. 1.23 (Hammer et al. 2001). Species
diversity is the total number of species observed in eachsample, while the Shannon–Wiener index is a measureof diversity that have in consideration also the amount ofcells.

39

are Syracosphaera molischii, Syracosphaera pulchra
and Syracosphaera ossa. Rhabdosphaeraceae were well
represented with concentrations up to 1.5 x103 cells/l at
Stn HAS, 5m). Among them $OJLURVSKDHUDUREXVWD and
5KDEGRVSKDHUDFODYLJHUD were the most prevalent. Helicosphaera carteri and Gephyrocapsa oceanica showed amaximum abundance 2.6 x102 cells/l in stations HAS, 5m
and M2, 3m respectively.

4. Discussion and conclusions
Elefsis Bay is a shallow semi-closed embayment(maximum depth 33 m) that presents a typically seasonalvariation of the hydrological parameters. The annual
3 Results
maximum average temperature occurs around July/
August (25o C); minimum values (10o C) are reached in
3.1 The semi-closed Elefsis Bay
February/March. Salinity shows an almost homogeneous
The total coccolithophore density in the Elefsis Bay
YHUWLFDO SURÀOH ZLWK VHDVRQDO YDULDWLRQ UDQJLQJ IURP
3samples was relatively low - 4.6 and 5.1 x10 coccospheres/l37.5 in March to 39.0 in summer (e.g., Friligos, 1983;(Table 2). The coccolithophore assemblage consisted only
Siokou-Frangou et al., 1998). During summer, the bay isof four heterococcolithophore species, with low speciesLQÁXHQFHGE\DSHUVLVWHQWWKHUPRFOLQHZKLFKGHYHORSVDW
diversity, but the Shannon–Wiener index was relative P OHDGLQJ WR ZDWHU FROXPQ VWUDWLÀFDWLRQ DQG FRQVHhigh (H=0.81 and 0.90), since no one species dominatedquent bottom-water anoxia, while intense vertical mixing
the assemblages.
of the water column occurs during winter (e.g., Scoullos
The most abundant species was Helicosphaera carteri
and Riley, 1978; Zarkanellas, 1979; Papathanasiou and3with concentrations up to 2.7 x10 coccospheres/l, thus
Zenetos, 2005). In addition to water mass circulation,
constituting more than 50% of the assemblage. No loose
the increased levels of domestic, industrial and shipping
helicoliths have been observed in the studied samples;
activities are continuously degrading the environmental
in general, the absence of loose helicoliths from thequality, especially associated with eutrophic conditions
samples indicates the new development of the popula(e.g., Friligos, 1981; Pagou, 1995; Pavlidou et al., 2010;tion (e.g., van der Waal et al., 1995). Emiliania huxleyi
Pavlidou, 2012), high values of hydrocarbons and trace
represents the second most abundant species that contribelements (e.g., Scoullos et al., 2007; Sklivagou et al.,3utes with 2.0x10 cells/l, comprising about 40% of the2008; Valavanidis et al., 2008). Particularly, the trophic
assemblage. Among the minor species, Gephyrocapsa
VWDWXVLVFKDUDFWHUL]HGDVHXWURSKLFIRUQLWUDWHaƫ0
oceanica ZDV D VLJQLÀFDQW HOHPHQW ZLWK FHOO GHQVLW\
DQG KLJKHU PHVRWURSKLF IRU SKRVSKDWH a  ƫƓ DQG2
up to 2.9 x10 coccospheres/l, whereas Syracosphaera
ammonium: ~ 1.12 (Pavlidou, 2012) have a prevailing2
anthos was present with cell densities less than 1.0 x10
control on the seasonal succession of phytoplankton (e.g.,
coccospheres/l (Table 2).
Ignatiades, 1983; Gotsis-Skretas, 1995; Pagou, 1995)
DQGVLJQLÀFDQWO\GHFUHDVHWKH]RRSODQNWRQULFKQHVV HJ
3.2 Off-shore environments of the AeSimboura et al., 1995; Siokou-Frangou et al., 1995, 1998).
gean Sea
In the present study, the late-winter coccolithophore
During winter and early spring the total coccosphereassemblages in the restricted environment of Elefsis Bay
densities from the studied Aegean Sea off-shore enviVKRZVLJQLÀFDQWO\ORZHUDEXQGDQFHDQGVSHFLHVGLYHUVLW\ronments varied between 9.2 x103 (central Aegean, Stnin comparison with off-shore assemblages of the Aegean3T1-8, 0 m) to 37.5 x10 cells/l (North Aegean, M4, 10
Sea. This is consistent with the results by Gotsis-Skretas
3m) with an average of 24.5 x10 cells/l (Table 2). A total(1995) who reported the lowest phytoplankton densiof 60 (48 heterococcolithophores and 12 holococcolithoties in Elefsis Bay in February, in contrast to the more
SKRUHV VSHFLHVKDYHEHHQLGHQWLÀHG7KHDYHUDJHVSHFLHV
open marine environments of Saronikos Gulf that present
diversity was 13 species per sample, with highest values
maxima in March. Furthermore, the low coccolithophore(26 taxa) observed in the South Aegean (Stn HAS, 5m).
VSHFLHVGLYHUVLW\ 7DEOH PD\UHÁHFWWKHXQVWDEOHHQYLShannon–Wiener index showed similar patterns withronmental conditions in the coastal environments. Indeed,
species diversity (Hmax=1.42 at South Aegean, Stn HAS,
the assemblage consists mainly of the two species H.
5m).
carteri and E. huxleyi. Interestingly, the coccolithophore
Emiliania huxleyi was the most abundant species with
Shannon-Wiener index in the area is higher than in the3concentrations up to 35.4 x10 cells/l in the North Aegeanoff-shore environments of the Aegean Sea during the(Stn M4, 10m), typically constituting >70% of the coccosame season (Table 2). From the statistical point of view,
lithophore assemblages. Syracosphaera spp. (up to 3.8
the high Shannon-Wiener index values are due to both H.
3x10 coccospheres/l at Stn M3) were generally represented
carteri and E. huxleyi high concentrations, while in the off
by more than 15 species, among which the most abundant

40&RFFROLWKRSKRUHV$EVWUDFWV

Plate 1Morphological variability in the coccoliths of Helicosphaera carteri (Wallich 1877) Kamptner 1954. fig. 1. Coccosphere with helicoliths having one longitudinal slit or two small pores in the central area, arranged along the long axisof the coccolith, Stn HAS 5m, fig. 2. Coccosphere with helicoliths having one or two longitudinal slits in the centralarea, arranged along the long axis of the coccolith; one coccolith having two oblique slits (arrow), Stn T1-3-5m, figs 3,
4. Coccosphere with helicoliths having one or two longitudinal slits in the central area, Stn S 5 m.

shore Aegean coccolithophore Shannon-Wiener index islower due to the dominance of E. huxleyi.
The opportunistic species E. huxleyi is by far the mostabundant coccolithophore on a global basis and has a wideecological distribution (e.g., Young, 1994). In the Mediterranean Sea waters, this species prevails throughout
the year in the living coccolithophore assemblages (e.g.,
Knappertsbusch, 1993; Kleijne, 1993; Cros, 2001; Malinverno et al., 2003; Triantaphyllou et al., 2004, 2010), andpredominates during winter in the Aegean Sea (Dimiza
et al., 2008a, b). In Elefsis Bay, it has been reported as
one of the most abundant species in the July peak of
microplankton abundance, with concentrations up to 3.1
x106 cells/l, constituting more than 70% of the population (Gotsis-Skretas, 1995; microplankton countings withinverted microscope).
Helicosphaera carteri has been rarely reported fromthe North Aegean, whereas it is a common minor compo-

nent of the assemblages of the South Aegean Sea (e.g.,
Triantaphyllou et al., 2004). However, its abundance inthe restricted environment of Elefsis Bay is unusuallyhigh, replacing in dominance E. huxleyi. In addition , H.
carteri coccospheres display notable morphological variability. Most helicoliths have two longitudinal slits in thecentral area, arranged along the long axis of the coccolith, however helicoliths with two clockwise oblique slits
or RQH ORQJLWXGLQDO VOLW DUH DOVR REVHUYHG 3ODWH  ÀJV
1-4). Traditionally, H. carteri, H. wallichii and H. hyalina
have been considered as varieties, since different coccoliths mostly based on the slits type in the central area,
have been recovered in association on the same coccosphere (Jordan and Young, 1990; Kleijne, 1993; Jordan
and Green, 1994; Cros and Fortuño, 2002; Malinverno
et al., 2008; present study). However, culture studies andmolecular analysis showed that coccolith morphology isstable in culture and that strains of the different morphot-

&RFFROLWKRSKRUHV$EVWUDFWV

41

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Helicosphaera carteri is commonly found in warm
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IUHTXHQFLHV LQ UHJLRQV LQÁXHQFHG E\ ULYHULQH GLVFKDUJH
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et al. (2005), when studying Holocene sediment records.
2XUUHVXOWVUHLQIRUFHWKHVHÀQGLQJVYHULI\LQJWKHRSSRUtunistic behavior of H. carteri in water samples, thus
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data, abnormal concentrations in nutrients and/or othertrace elements, measured in the same water samples is
HVVHQWLDOWRFRQÀUPWKHVHUHVXOWV'HWDLOHGIXWXUHUHVHDUFK
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