Content uploaded by Muhammet TÜRKOĞLU
Author content
All content in this area was uploaded by Muhammet TÜRKOĞLU
Content may be subject to copyright.
Provided for non-commercial research and educational use only.
Not for reproduction or distribution or commercial use.
This article was originally published by IWA Publishing. IWA Publishing recognizes
the retention of the right by the author(s) to photocopy or make single electronic
copies of the paper for their own personal use, including for their own classroom use,
or the personal use of colleagues, provided the copies are not offered for sale and
are not distributed in a systematic way outside of their employing institution.
Please note that you are not permitted to post the IWA Publishing PDF version of
your paper on your own website or your institution’s website or repository.
Please direct any queries regarding use or permissions to hydrology@iwap.co.uk
Winter bloom of coccolithophore Emiliania huxleyi
and environmental conditions in the Dardanelles
Muhammet Turkoglu
ABSTRACT
Muhammet Turkoglu (corresponding author)
Fisheries Faculty, Hydrobiology Department,
Canakkale Onsekiz Mart University,
Terzioglu Campus,
17100 Canakkale,
Turkey
Tel.: +902862180018-1572
Fax: +902862180543
E-mail: mturkoglu@comu.edu.tr
Following a summer bloom of coccolithophore Emiliania huxleyi (Lohmann) Hay & Mohler, 1967,
in 2003, a winter bloom was observed for the first time between late December 2003 and early
January 2004 in the Dardanelles. Microscopic observations showed that the cell dimensions of
E. huxleyi (Ehux) varied from 9.85 to 13.50 mm in diameter (mean: 11.20 ^ 1.38 mm). While Ehux
revealed a relatively small population density (1.60 £ 10
4
cells L
21
) in early December 2003, the
bloom started in middle December 2003 (7.86 £ 10
6
cells L
21
) and then peaked in early January
2004 (5.03 £ 10
7
cells L
21
) in the superficial layer. The peak dramatically decreased in late January
2004 (7.50 £ 10
6
cells L
21
). Ehux was the dominant species and represented about 90.0% of the
phytoplankton assemblage. The bloom started flourishing after the diatom and dinoflagellate
blooms under nitrogen depletion and moderate light, temperature and salinity conditions.
Water temperature (10.31 ^ 1.148C) and salinity values (27.05 ^ 0.88 ppt) were usually stabile.
Surface chlorophyll-a concentrations ranged from 1.23 to 2.32 mgL
21
during the bloom. The ratios
of N:P (mean: 4.12 ^ 2.22) and Si:P (40.35 ^ 16.25) of the bloom period were lower than those
of the non-bloom periods.
Key words
|
algal blooms, Dardanelles, Emiliania huxleyi, environmental factors, winter
INTRODUCTION
Except for the polar oceans, E. huxleyi (Ehux) is one of the
most abundant coccolithophores occurring globally in the
entire oceans in early summer periods. This species drifts
freely and prefers the surface layers of the oceans. It has
received considerable attention since it tends to produce
massive blooms under favorable conditions (Balch et al.
1991, 1992; Tyrrell & Taylor 1995; Nanninga & Tyrrell 1996;
Hattori et al. 2004; Smyth et al. 2004; Turkoglu 2008). In
summer, high surface irradiance, shallow stratification with
a mixed layer depth of about 10–20 m, anomalies in salinity
and temperature, and low phosphate and silicate concen-
trations favor the bloom of this species (Egge & Heimdal
1994; Tyrrell & Taylor 1995; Nanninga & Tyrrell 1996;
Smyth et al. 2004; Zeichen & Robinson 2004).
In recent years, satellite images have revealed surprising
bright expanses of water in some marine systems such as the
eastern Bering Sea in the middle of winter. Similar bright
waters occur in summer and have been identified as blooms
of the coccolithophore Ehux. However, Ehux blooms are
an unlikely cause of the bright waters in winter because
hostile conditions should prevent extensive phytoplankton
blooms (Broerse et al. 2003).
However, Sorrosa et al. (2005) clearly showed that low
temperature suppresses coccolithophorid growth but
induces cell enlargement and stimulates the intracellular
calcification that produces coccoliths. For instance, while
coccolithophore Ehux grows at a wide temperature
range (10–258C), another coccolithophore Gephyrocapsa
oceanica Kamptner, 1943 grows at a narrow temperature
range (20–258C) and cell size is inversely correlated with
temperature (Sorrosa et al. 2005). At low temperature, the
enlargement of chloroplasts and cells and the stimulation
doi: 10.2166/nh.2010.124
104 Q IWA Publishing 2010 Hydrology Research
|
41.2
|
2010
of coccolith production have been morphologically
confirmed under fluorescent and polarization microscopes
(Sorrosa et al. 2005). The uptake of
45
Ca by Ehux at 108C
has been greatly increased after a five-day lag and exceeded
that at 208C(Sorrosa et al. 2005). During the blooms, the
numbers of Ehux cell densities usually outnumber those of
other species, frequently accounting for about 80% or more
of the total number of phytoplankton cells (Turkoglu 2008).
One important matter of blooms of Ehux is that it alters
the ecological conditions of a marine system by acting as a
source of organic sulfur (i.e. dimethyl sulfide) to the
atmosphere (Balch et al. 1992; Burkill et al. 2002) and
calcium carbonate to the sediments (Balch et al. 1996;
Tekiroglu et al. 2001). Moreover, high cell densities can
provoke the water to change to a milky white or turquoise
color due to significant changes in the inherent optical
properties of water (Brown & Yoder 1994; Cokacar et al.
2001, 2004; Smyth et al. 2004; Turkoglu 2008). Besides, as a
consequence of blooms the coccolithophore are now
receiving greater attention, as their role in the global sulfur
and carbon cycles may influence the world’s climate and
their potential as nuisance bloom algae have implications
for commercial fishing and the marine ecosystem (Jordan &
Chamberlain 1997). Therefore, documenting the occurrence
of blooms in time and space is essential to characterize the
biogeochemical environment of a target region. Studies on
coccolithophore Ehux by Turkoglu et al. (2004b,c) and
Turkoglu (2008) have also indicated advancing of this
species from the Black Sea region through the Sea of
Marmara and the Dardanelles under favorable conditions.
Phytoplankton species succession in the Turkish Straits
System which contains the Bosphorus, Dardanelles and Sea
of Marmara shows similarities to the succession in the
Black Sea (Koray et al. 2000; Turkoglu & Koray 2000, 2002).
The time sequence of SeaWiFS images shows the develop-
ment of the Ehux bloom in the Sea of Marmara in the
early summer of 2003. In the images, the turquoise color
indicates the regions with the highest coccolith accumu-
lations. During the early summer bloom period, the cell
density of Ehux increased from 3.58 £ 10
7
to 2.55 £ 10
8
cells L
21
in the superficial layer. Between 12 June and
25 June, Ehux exceeded 2.0 £ 10
8
cells L
21
in the super-
ficial layer (Turkoglu et al. 2004b,c; Turkoglu 2008). In
addition to blooms of Ehux in the early summer periods, the
system was also controlled by dinoflagellates such as
Ceratium spp. and Prorocentrum spp. during the year and
diatoms such as Proboscia alata (Brightwell) Sundstro¨m,
1986, Pseudo-nitzschia pungens (Grunow ex P.T. Cleve)
Hasle, 1993 and Dactyliosolen fragilissimus (Bergon) G. R.
Hasle, 1991 in winter, spring and late summer periods
(Unsal et al. 2003; Turkoglu et al. 2004b–d). Researchers
have reported harmful and toxic algal blooms such as
Dinophysis spp. and Gonyaulax spp. that potentially threat
the region (Unsal et al. 2003; Turkoglu et al. 2004b–d).
The main target of this study is to exhibit the bloom
circumstances and the reasons of coccolithophore Ehux
along with environmental conditions in winter period in the
Dardanelles. Environmental characteristics, hydrographic
structure, inorganic nutrients and chlorophyll-a have been
investigated in relation to the blooms of the Dardanelles.
This study reports the winter bloom of Ehux in the
Dardanelles and interactions of this species with other
phytoplankton species in response to environmental
parameters for the first time.
MATERIALS AND METHODS
The Dardanelles is a very important water passage
connecting the Aegean Sea to the Sea of Marmara. It has
two current systems; one of the currents derives from the
Aegean Sea, where the water density is high, and the second
one comes from the Sea of Marmara, characteristically low
in density. Aegean Sea water is typically flowing from the
southwest (SW) to northeast (NE) below the Sea of
Marmara water. Its NE/SW trend is interrupted by a
north–south bend between Eceabat and Canakkale. In
addition to the first bend, there is a second bend called the
“Nara Cape”. The width of the Strait varies from 1.35 to
7.73 km and the narrowest part is located between
Canakkale and Kilitbahir. The average depth of the Strait
is approximately 60 m, with the deepest part reaching more
than 100 m (Unsal et al. 2003; Turkoglu et al. 2004c, 2006;
Baba et al. 2007). However, the depth of the study area in
the Dardanelles is 80 m. The location of the sampling
station (40809
0
00
00
N26824
0
00
00
E) is given in Figure 1.
Water samples for nutrient analyses, phytoplankton
enumeration and chlorophyll-a estimation were collected
105 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
by a Niskin Sampling Bottle from depths of 0.5, 10, 25, 50
and 75 m in the Dardanelles (40809
0
N, 26824
0
E) (Figure 1)
in a 10-day interval between December 2003 and January
2004. Sea temperature, salinity, pH and dissolved oxygen
(DO) were measured in situ using an YSI 6600 Model
Multiple Water Analysis Probe.
Water samples for nutrient analyses were kept frozen
until analysis. Analysis for nitrite þ nitrate ðNO
2
2
þ NO
2
3
Þ,
inorganic phosphate ðPO
23
4
Þ and silicate (SiO
4
) were
measured using a Technicon model auto-analyzer accord-
ing to Strickland & Parsons (1972).
Chlorophyll-a samples were filtered through GF/F glass
fiber filters. The filters were folded into aluminum foil and
immediately frozen for laboratory analysis. Chlorophyll-a
was determined spectrophotometrically after extraction by
90% acetone (Strickland & Parsons 1972).
For the quantitative analysis of phytoplankton, samples
were preserved with 2% buffered formalin (v/v) and
microscopic analysis was conducted within a week of
collection. Utermo¨ hl Sedimentation Chambers and Neu-
bauer and Sedgwick Rafter Counting Slides were used in
combination for enumeration of the phytoplankton species,
depending on the dimensions and concentrations of the
organisms (Guillard 1978; Hasle 1978; Venrick 1978).
Pearson correlation analysis and paired samples’ t test
were conducted using SPSS 11.5 (SPSS 2003). In some
cases linear regression relationships were also obtained. All
variables except pH were previously log
10
transformed to
improve linearity, normality and homogeneity of variances
(Quinn & Keough 2002).
RESULTS
Physical variables
Vertical profiles of temperature and salinity suggested that
there were two different water masses during the Ehux
winter bloom (Figure 2(A, B)). During the winter period,
salinity values in the upper layer between 0 and 10 m,
an intermediate layer between 10 and 50 m and a lower
layer between 50 and 75 m varied between the values of
25.72–27.77, 26.28–37.67 and 38.31–38.75 ppt, respect-
ively (Figure 2(B)). Both seasonal reverse thermocline and
halocline interfaces were clear due to the two different
Figure 1
|
Map of the sampling station in the Dardanelles.
Figure 2
|
The vertical profiles of temperature (A), salinity (B), pH (C) and dissolved
oxygen (DO) (D) in winter in the Dardanelles.
106 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
water layer systems and formed between 25 and 50 m in
the non-bloom period (before bloom and after bloom) and
between 10 and 50 m in the bloom period of Ehux (Table 1
and Figures 2(A, B)).
During the Ehux winter bloom, pH changed from 6.61
to 8.67 in the upper layer and from 7.17 to 8.79 in the lower
layer (Figure 2(C)). DO values in both the upper (8.04–
11.95 mg L
21
) and the lower layer (7.16–9.17 mg L
21
)of
the Dardanelles revealed high saturation (Figure 2(C)). DO
concentrations gradually decreased from the upper super-
ficial layer to the lower layer during the winter bloom.
Nutrient behaviors
Vertical profiles of inorganic nutrients showed that the
concentrations in the upper layer were generally lower than
those in the lower layer during winter bloom conditions
(Figure 3(A–C)). There was a decrease in concentration of
NO
2
2
þ NO
2
3
(0.11–0.28 mM) at 10 m in the vertical profile.
Under 10 m, NO
2
2
þ NO
2
3
gradually increased with depth
(0.16–0.61 mM), while PO
23
4
was generally resistant to
change with depth (0.05–0.09 mM) except that there was
a small increase at 25 m (0.05–0.12 mM). SiO
4
concen-
trations changed between 1.40 and 4.25 mM in the upper
layer during the winter Ehux sampling period, but they were
below concentrations of 2.00 mM during the Ehux bloom
except for the value recorded on 2 January 2004 (3.03 mM)
when a peak value in cell density of Ehux was observed.
However, they increased slowly with depth (2.21 –3.50 mM)
except for the vertical SiO
4
profile recorded on 29
January 2004. SiO
4
decreased with depth on this date
(3.05–4.25 mM) (Figure 3(C)).
The ratios of N:P were significantly lower (2.00–7.33)
(Figure 3(D)) than the assimilatory optimal of the Redfield
ratio (N:P ¼ 16.0). On the other hand, there was a
decreasing profile in the ratios of Si:P between the lower
layer and the upper layer (Figure 3(E)). The ratios of N:P
ranged from 1.83 to 10.90 (Figure 3(D)), while the ratios of
Si:P ranged from 17.1 to 62.2 in both the upper layer and
the lower layer during the bloom conditions (Figure 3(E)).
Succession of E. huxleyi and other phytoplankton groups
Results of microscopic observation clearly showed that
cell dimensions of Ehux varied between 9.85 and 13.50 mm
in diameter (mean: 11.20 ^ 1.38 mm) (Table 1). Although
there was an important development of the Ehux
bloom (Figure 4(A)) in the Dardanelles, there was
no apparently turquoise or bright color change in the
system in early winter (December, 2003) and mid-winter
Table 1
|
Descriptive statistics of biological, physical, and chemical data groups in the surface layer (0.5 m) of the Dardanelles
N Min Max Mean SD
Temperature (8C) 6 9.06 12.30 10.31 1.14
Salinity (ppt) 6 25.72 27.67 27.05 0.88
pH 6 6.61 8.31 7.61 0.64
DO (mg L
21
) 6 8.04 11.95 10.10 1.31
NO
2
2
þ NO
2
3
(mM) 6 0.10 0.44 0.26 0.14
PO
23
4
(mM) 6 0.05 0.08 0.06 0.01
SiO
4
(mM) 6 1.40 4.25 2.51 1.16
N:P 6 2.00 7.33 4.12 2.22
Si:P 6 24.00 58.50 40.35 16.25
Chl-a (mgL
21
) 6 1.23 2.32 1.94 0.43
Dinoflagellates (cell L
21
) 6 1.65 £ 10
5
4.41 £ 10
6
1.77 £ 10
6
1.41 £ 10
6
Diatoms (cell L
21
) 6 3.93 £ 10
5
1.20 £ 10
7
4.20 £ 10
6
4.29 £ 10
6
E. huxleyi (cell L
21
) 6 1.60 £ 10
4
5.03 £ 10
7
2.08 £ 10
7
1.86 £ 10
7
E. huxleyi cell diameter (mm) 35 9.85 13.50 11.25 1.45
Notes: N, sampling number; Min, minimum value; Max, maximum value; SD, standard deviation.
107 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
(January, 2004). The algal bloom started to improve
towards the middle of December, then reached a maximum
value (5.03 £ 10
7
cells L
21
)(Figure 4(A)) in early January
(2 January 2004) and afterward lost out its advantage in late
January (7.50 £ 10
6
cells L
21
versus 1.20 £ 10
7
cells L
21
)
(Figure 4(C)).
Vertical profiles of Ehux (Figure 4(A)) revealed that
its cell density increased from 1.60 £ 10
4
to 5.03 £ 10
7
cells L
21
in the upper layer. In early January, Ehux exceeded
5.00 £ 10
7
cells L
21
in the upper layer. However, the
density dramatically decreased with depth. For instance,
the cell concentration declined from 5.03 £ 10
7
in the
upper layer to 1.76 £ 10
5
cells L
21
in the lower layer
(Figure 4(A)). The cell density of dinoflagellates and
diatoms showed that there was no effect of Ehux on the
development of dinoflagellates, although there was an effect
of Ehux on the development of diatoms. There were also
high densities of dinoflagellates (1.0 £ 10
6
–4.41 £ 10
6
cells L
21
)(Figure 4(B)) contributed by Prorocentrum spp.
and Ceratium spp. in the upper layer during the Ehux
winter bloom period. However, diatoms were at minimum
density values just before and at the time of the Ehux winter
bloom peak value ( Figure 4(C)). Afterwards, diatoms such
as Leptocylindrus spp., P. pungens, and D. fragilissimus
started to increase due to the loss of Ehux bloom effort and
their excessive cell densities exceeded a value of 1.00 £
10
7
cells L
21
in the upper layer in late January (Figure 4(C)).
The density of diatoms reached 2.10 £ 10
7
cells L
21
, which
was the maximal bloom value in the sub-surface (10 m)
during the bloom period (Figure 4(C)).
Ehux was found to be the dominant species, accounting
for more than 90.0% of the phytoplankton assemblage
in the middle of the bloom (Table 2 ). Diatoms (5.92%)
and dinoflagellates (3.99%) were other important
Figure 3
|
The vertical profiles of NO
2
2
þ NO
2
3
(A), PO
23
4
(B), SiO
4
(C), N:P (D) and Si:P
ratios (E) in winter in the Dardanelles.
Figure 4
|
The vertical profiles of E. huxleyi (A), dinoflagellates (B), diatoms (C), total
phytoplankton (D) and chlorophyll-a (E) in winter in the Dardanelles.
108 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
taxonomic groups during the Ehux bloom (Table 2). While
the largest contribution to diatoms came from species of
Leptocylindrus spp., P. pungens and D. fragilissimus, the
largest contribution to dinoflagellates came from species
of Prorocentrum spp. (especially Prorocentrum micans
Ehrenberg, 1834, the most opportunist one) and Ceratium
spp. such as Ceratium furca (Ehrenberg, 1834) Clapare
`
de et
Lachmann, 1859 and Ceratium fusus (Ehrenberg, 1834)
Dujardin, 1841 according to their cell density order.
While cell densities of the diatoms and dinoflagellates
in the superficial layer varied between 1.65 £ 10
5
and
4.41 £ 10
6
cells L
21
and between 3.93 £ 10
5
and 1.2 £ 10
7
cells L
21
, respectively, their densities in the sub-surface
layer varied between 8.33 £ 10
5
and 1.66 £ 10
6
cells L
21
and between 7.07 £ 10
5
–2.1 £ 10
7
cells L
21
, respectively.
Except for the 29 January 2004 sampling date on which
Ehux algal bloom highly decreased (7.5 £ 10
6
cells L
21
),
the cell density of diatoms was below 5.0 £ 10
6
cells L
21
in
the superficial layer (0.5 m) due to the fairly high Ehux
bloom (1.60 £ 10
7
–5.03 £ 10
7
cells L
21
), and was above
1.0 £ 10
7
cells L
21
both in the surface layer (0.5 m) and
in the sub-surface layer (10 m) in the last of the bloom
(Figure 4(C)) due to the more dramatic decrease of the
Ehux bloom (Figure 4(A)). However, the highest diatom
production was in the surface and sub-surface layers due
to a sufficient amounts of nutrients, especially silicate
(. 3.00 mM) (Figure 3(A–C)) and the dramatic decrease
of the Ehux bloom (Figure 4(A)). This tendency of diatoms
in the vertical profile was roughly similar to the vertical
profile of the dinoflagellates which were less than diatoms
(Figure 4(B, C)).
Phytoplankton chlorophyll-a
Chlorophyll-a concentrations ranged from 1.23 to
2.32 mgL
21
(1.94 ^ 0.43) in the upper layer where there
was an Ehux bloom (Table 1 and Figure 4(E)). However,
chlorophyll-a maximal values were also observed in the
sub-surface layer (10 m) due to diatom and other blooms at
this depth during the bloom period (Figure 4(E)).
Comparative interactions
In regard to comparative interactions, analysis revealed that
there was no significant relationship between Ehux and
PO
23
4
(Figure 5). Dinoflagellates showed strong negative
correlations with SiO
4
in the surface layer (Table 3).
Additionally, strong positive relations were observed
between dinoflagellates and PO
23
4
in the surface layer.
Diatoms were strongly correlated with temperature, pH,
PO
23
4
and SiO
4
in the interface layer (Table 3).
Because there were no high cell densities of Ehux in the
bloom period, nutrients (NO
2
2
þ NO
2
3
,PO
23
4
and SiO
4
) and
their proportional relations (N:P and Si:P ratios) were more
correlated with dinoflagellates and diatoms rather than with
Ehux in both the surface and the deep layer (Table 3).
Table 2
|
Rational contributions (%) of dinoflagellates, diatoms and coccolithophore E. huxleyi to total phytoplankton in the different water layers of the Dardanelles
Date Stratification Depth Dinophyceae Bacillariophyceae E. huxleyi
04.12.03 19.12.03 29.12.03 04.12.03 19.12.03 29.12.03 04.12.03 19.12.03 29.12.03
Dec. 03 Upper layer 0.5 65.43 9.97 3.99 33.84 2.19 5.92 0.72 87.49 90.09
10 45.14 8.80 8.80 53.95 7.48 15.20 0.91 83.06 76.00
Intermediate layer 25 26.35 8.91 8.38 73.65 13.18 22.72 0.00 77.33 68.90
Lower layer 50 13.98 5.63 7.22 81.10 23.94 31.20 0.00 70.42 61.58
75 13.25 19.08 20.06 86.75 37.57 53.19 0.00 43.35 26.75
02.01.04 16.01.04 29.01.04 02.01.04 16.01.04 29.01.04 02.01.04 16.01.04 29.01.04
Jan. 04 Upper layer 0.5 2.24 17.27 0.84 8.28 20.05 61.02 89.49 62.67 38.14
10 2.78 17.33 5.65 24.20 48.79 87.87 66.09 33.88 6.49
Intermediate layer 25 3.83 50.99 7.71 21.53 35.90 84.11 71.90 13.11 8.18
Lower layer 50 11.85 43.91 17.85 28.89 38.95 70.99 55.63 17.14 11.16
75 21.97 33.33 34.55 54.59 55.56 65.45 23.44 11.11 0.00
109 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
However, negative relationship between Ehux and PO
23
4
was not statistically significant (Table 3 and Figure 5) due
to the fact that PO
23
4
was assimilated by high diatom
production during the long time period before the bloom
of Ehux. Therefore, there were lower concentrations of
PO
23
4
in that period.
In the upper layer, positive correlations between
chlorophyll-a and Ehux (R ¼ 0.330), between chlorophyll-a
and dinoflagellates (R ¼ 0.350) and between chlorophyll-a
and total phytoplankton (R ¼ 0.247) were more impor-
tant than the correlation between chlorophyll-a and
diatoms (R ¼ 0.090) due to competition between diatoms
and Ehux (Table 3).
DISCUSSION
Insufficient inorganic nutrients, especially reactive phos-
phate due to extensive utilization of them by diatoms just
before the Ehux algal bloom, high irradiance and so
high temperature, and a stable water column in terms of
vertical mixing following the establishment of the seasonal
thermocline were the characteristics of the Ehux summer
bloom in the Dardanelles (Turkoglu 2008), confirming
previous studies on Ehux blooms in the North Sea and NE
Atlantic (Nanninga & Tyrrell 1996; Smyth et al. 2004;
Zeichen & Robinson 2004). In general, it has been suggested
that Ehux blooms follow the blooms of diatoms in marine
system (Holligan et al. 1993; Uysal 1995; Turkoglu & Koray
2002, 2004; Broerse et al. 2003; Cokacar et al. 2004; Turkoglu
et al. 2004b; Turkoglu 2005, 2008; Oguz & Merico 2006).
Figure 5
|
Relationships between E. huxleyi and PO
23
4
in the upper layer (0.5 m),
intermediate layer (25 m) and lower layer (50 m) of the Dardanelles. For
each regression, the coefficients of determination ( R
2
) and the process of
equating (y ) are shown.
Table 3
|
Pearson correlation coefficients for the relationship between physicochemical
and biological data groups in the Dardanelles
Dinop Bacil Ehux Phyto
Upper layer
Temperature 2 0.111 2 0.776 2 0.265 2 0.450
Salinity 2 0.134 2 0.840
p
0.440 0.236
pH 0.051 0.827
p
0.060 0.251
DO 0.183 2 0.554 0.844
p
0.727
NO
2
þ NO
3
0.356 0.742
p
0.169 0.364
PO
23
4
2 0.357 0.681 2 0.338 2 0.207
SIO
4
2 0.088 0.957
†
0.055 0.266
N:P 0.500 0.517 0.349 0.502
Si:P 0.116 0.724 0.323 0.495
Chl-a 0.350 0.090 0.330 0.247
Intermediate layer
Temperature 2 0.601 2 0.599 0.190 2 0.492
Salinity 2 0.727 2 0.617 0.463 2 0.266
pH 0.469 0.682 2 0.637 0.106
DO 0.901
p
2 0.193 2 0.250 2 0.218
NO
2
þ NO
3
0.320 0.362 2 0.178 0.239
PO
23
4
2 0.037 0.296 2 0.208 0.046
SiO
4
0.357 0.589 2 0.386 0.251
N:P 0.232 0.043 0.082 0.195
Si:P 0.134 2 0.045 0.123 0.131
Chl-a 2 0.209 2 0.307 0.471 0.160
Lower layer
Temperature 2 0.616 2 0.475 0.093 2 0.149
Salinity 2 0.806 0.003 0.092 2 0.062
pH 0.501 0.151 2 0.497 2 0.240
DO 0.729 2 0.178 2 0.326 2 0.165
NO
2
þ NO
3
0.795 0.749 0.202 0.473
PO
23
4
2 0.269 0.141 0.165 0.093
SiO
4
0.805 0.567 2 0.005 0.279
N:P 0.871
p
0.667 0.157 0.437
Si:P 0.758 0.276 2 0.089 0.145
Chl-a 0.343 0.585 0.705 0.737
p
Significant at
a
¼ 0.05.
†
Significant at
a
¼ 0.01.
N ¼ 6.
110 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
There was an extensive bloom of Ehux (5.03 £ 10
7
cells L
21
) in spite of deficient irradiance and temperature.
However, this bloom was lower than that of the 2003
summer bloom (2.55 £ 10
8
cells L
21
)(Turkoglu 2008),
probably due to insufficient irradiance and temperature
(min–max: 9.06–12.30; mean: 10.31 ^ 1.148C). Notwith-
standing, results of microscopic observations clearly
showed that cell dimensions of Ehux in the winter bloom
period (min–max: 9.85–13.50 mm in diameter; mean:
11.20 ^ 1.38 mm) were bigger in diameter than the cell
dimensions in the summer bloom period (min–max: 7.86–
12.37 mm in diameter; mean: 9.05 ^ 1.05 mm) in the
Dardanelles (Table 4). According to the “paired samples’
t test”, the difference between winter and summer mean
values in cell diameters of E. huxleyi was important at a
level of “p , 0.01” (Table 4). Regarding correlations
between Ehux and CTD parameters, there were some
supportable relationships. Ehux were weakly related with
temperature (R ¼ 2 0.265), salinity (R ¼ 0.440) and pH
(R ¼ 0.060), but strongly with DO (R ¼ 0.844) in the upper
layer (Table 3). However, a negative relationship between
Ehux and temperature during the winter bloom was
supported by Sorrosa et al. (2005). They clearly revealed
that low temperature suppresses coccolithophorid growth
but induced cell enlargement and stimulated the intra-
cellular calcification that produces coccoliths. They also
showed that Ehux grew at a temperature range between 10
and 258C and its cell size was inversely correlated with
temperature. At low temperature, the enlargement of
chloroplasts and cells and the stimulation of coccolith
production have been morphologically confirmed under
fluorescent and polarization microscopes, respectively
(Sorrosa et al. 2005).
In this study, although the maximum density of Ehux
was lower (5.03 £ 10
7
cells L
21
) in the 2003–2004 winter
period (Figure 4(A)) than the maximum density in the 2003
summer period (2.55 £ 10
8
cells L
21
)(Turkoglu 2008), the
contribution of Ehux to the total phytoplankton in the peak
of the bloom time (29 December 2003) was similar
(90.09%) (Table 2) to the contribution of Ehux in the
2003 summer period (97.58%) (Turkoglu et al. 2004b;
Turkoglu 2008). It is known that, during Ehux bloom
periods, the contribution of Ehux to total phytoplankton
usually outnumbers the contribution of other taxonomic
groups to total phytoplankton, frequently accounting for
about 80% or more of the total phytoplankton cell densities
(Cokacar et al. 2004; Turkoglu et al. 2004b; Turkoglu 2008).
Nutrient behavior during the Ehux winter bloom was
similar to the one that occurred during the summer period
(Turkoglu 2008). It was reported that nutrient dynamics
in the Dardanelles differed slightly due to different water
masses (Polat & Tugrul 1995; Unsal et al. 2003; Turkoglu
et al. 2004a,c,d; Turkoglu & Erdog
˘
an 2007a,b; Turkoglu
et al. 2007; Turkoglu 2008). Insufficient nutrient concen-
trations, especially silicate (1.40–2.03 mm) in the surface
layer rather than in the deep layer (2.10–3.50 mm) was
likely due to the utilization of nutrients by the early diatom
blooms. However, diatoms were found in low densities in
Table 4
|
Paired samples’ t test between winter and summer mean values in cell diameters of E. huxleyi
Paired samples’ statistics
Mean N Std. deviation Std. error mean
Pair 1 Summer 9.053 35 1.052 0.178
Winter 11.201 35 1.383 0.234
Paired samples’ correlations
N Correlation Sig.
Pair 1 Summer and winter 35 2 0.017 0.925
Paired samples’ test
Paired differences
95% confidence interval of the difference
Mean Std. deviation Std. error mean Lower Upper t df Sig. (two-tailed)
Pair 1 Summer–winter 2 2.148 1.751 0.296 2 2.750 2 1.546 2 7.256 34 0.000
111 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
the surface layer (0.5 m) and in the sub-surface layer (10 m),
except for the sampling date of 29 January 2004. While the
low diatom densities in the surface layer were affected by
Ehux bloom, they were probably affected by insufficient
irradiance in the sub-surface and deep layers (10–75 m).
Consequently, although there was sufficient nutrient con-
centration high enough to tolerate for diatom growth in the
lower layer during the Ehux winter bloom, the diatom
growth was quite insufficient in the lower layer due to some
ecological factors such as insufficient irradiance. However,
just after the Ehux bloom, there was a high diatom
production sourced by Leptocylindrus danicus P.T. Cleve,
1889 in the surface (0.5 m) (5.12 £ 10
6
–1.2 £ 10
7
cells L
21
) and the sub-surface layer (10 m) (4.68 £ 10
6
–
2.1 £ 10
7
cells L
21
) between 16 January and 29 January
2004 (Figure 4(C)). Some researchers revealed that
diatoms were favored when nitrogen was available at
higher concentrations (Piehler et al. 2004) and large
phytoplankton cells such as L. danicus, D. fragilissimus
and P. pungens were better competitors for nitrate because
of their larger specific storage volume (Dauchez et al. 1996;
Kormas et al. 2002).
In contrast to diatoms, Ehux is known to tolerate low
nutrients, especially low phosphate concentrations due to
its alkaline phosphatase enzyme and this talent permits this
group to outcompete other species (Balch et al. 1991;
Paasche 2002). On the other hand, the study area was
generally limited by nitrogen and the low N:P proportion in
the bloom period was in conformity with previously
reported values (Polat et al. 1998; Turkoglu et al.
2004a,c,d; Turkoglu & Erdog
˘
an 2007a,b; Turkoglu et al.
2007; Turkoglu 2008).
Redfield et al. (1963) calculated that C:N:P proportions
were in ratio of 106:16:1 in seawater. If N:P ratios in a
marine system are generally below the normal value of 16:1,
the system is limited by nitrogen (Stefanson & Richards
1963). However, if Si:N ratios in a system are below the
value of 1:1, the system is limited by silicate. Since N:P
proportions in the surface layer (min–max: 2.00–7.33;
mean: 4.12 ^ 2.22) were below the Redfield ratio (16:1) and
Si:N ratios (min–max: 24.00–58.50; mean: 40.35 ^ 16.25)
were above the Redfield ratio (1:1), the Dardanelles was
limited for nitrogen, but for phosphate and silicate. The fact
that the system was limited by nitrogen has been accepted
as the general situation not only for bloom periods but
for no bloom periods as well in all water columns for two
decade (Polat & Tugrul 1995; Polat et al. 1998; Turkoglu
et al. 2004c,d, 2007; Turkoglu 2008). It is known that
diatom increase in marine systems is likely to be limited
by dissolved reactive silica when Si:N ratios are less
than 1 according to the Redfield ratios (Redfield et al.
1963; Piehler et al. 2004) or N:Si ratios above 1 (Roberts
et al. 2003).
CONCLUSIONS
This work is the first attempt to present temporal and
vertical distribution of Ehux winter blooms and the
interaction of this species with other phytoplankton groups
in the same period in the Dardanelles. Previous studies
have shown summer blooms of this species in the Sea of
Marmara (Unsal et al. 2003; Turkoglu et al. 2004a–c;
Turkoglu et al. 2007; Turkoglu & Erdogan 2007a,b;
Turkoglu 2008) and in the Black Sea region since
the 1980s (Moncheva & Krastev 1997; Mikaelyan 1997;
Turkoglu & Koray 2002, 2004). Therefore, this study may
also indicate advancing of this species from the Black Sea
region through the Sea of Marmara and the Dardanelles
under favorable conditions. This may be due to climate
changes, in addition to the dramatic eutrophication of the
system since the 1980s. Nowadays, this species composes
not only extensive summer blooms but also winter blooms
in the Sea of Marmara. Unfortunately, this species seems
be able to create more extensive algal blooms in the
near future. Further monitoring of the system in terms of
anomalies in the temperature, salinity and nutrient changes
as well as the phytoplankton species composition is needed
for a better understanding of the ecological significance of
this species in this system and its neighboring systems,
the Black Sea and Northern Aegean Sea.
ACKNOWLEDGEMENTS
This study was supported by the Turkish Scientific and
Technical Research Council, Environmental, Atmospheric,
Earth and Marine Sciences Research Group (TUBITAK-
C¸ AYDAG, project no. 101Y081).
112 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
REFERENCES
Baba, A., Deniz, O., Turkoglu, M. & Ozcan, H. 2007 Investigation
of discharge of fresh water in the Canakkale Strait
(Dardanelles-Turkey). In: Linkov, I., Gregory, A. K. &
Richard, J. W. (eds) Environmental Security in Harbors and
Coastal Areas. Springer-Verlag, Berlin, pp. 421–427.
Balch, W. M., Holigan, P. M., Ackleson, S. G. & Voss, K. J. 1991
Biological and optical properties of mesoscale coccolithophore
blooms in the Gulf of Maine. Limnol. Oceanogr. 36, 629–643.
Balch, W. M., Holigan, P. M. & Kilpatrick, K. A. 1992 Calcification,
photosynthesis and growth of the bloom-forming
coccolithophore, Emiliania huxleyi. Cont. Shelf Res. 12,
1353–1374.
Balch, W. M., Kilpatrick, K. A., Holigan, P. M., Harbour, D. &
Fernandez, E. 1996 The 1991 coccolithophore bloom in the
central North Atlantic. 2. Relating optics to coccolith
concentration. Limnol. Oceanogr. 41, 1684–1696.
Broerse, A. T. C., Tyrrell, T., Young, J. R., Poulton, A. J., Merico, A.,
Balch, W. M. & Miller, P. I. 2003 The cause of bright waters in
the Bering Sea in winter. Cont. Shelf Res. 23, 1579–1596.
Brown, C. W. & Yoder, J. A. 1994 Coccolithophorid blooms in the
global ocean. J. Geophys. Res. 99, 7467–7482.
Burkill, P. H., Archer, S. D., Robinson, C., Nightingale, P. D.,
Groom, S. B., Tarran, G. A. & Zubkov, M. V. 2002 Dimethyl
sulphide biogeochemistry within a coccolithophore bloom
(DISCO): an overview. Deep-Sea Res. II 49, 2863–2885.
Cokacar, T., Kubilay, N. & Oguz, T. 2001 Structure of Emiliania
huxleyi blooms in the Black Sea surface waters as detected by
SeaWIFS imagery. Geophys. Res. Lett. 28, 4607–4610.
Cokacar, T., Oguz, T. & Kubilay, N. 2004 Satellite-detected early
summer coccolithophore blooms and their interannual
variability in the Black Sea. Deep-Sea Res. I 51, 1017– 1031.
Dauchez, S., Legendre, L., Fortier, L. & Levasseur, M. 1996 Nitrate
uptake by size-fractionated phytoplankton on the Scotian shelf
(Northwest Atlantic): spatial and temporal variability. J. Plank.
Res. 18, 577–595.
Egge, J. K. & Heimdal, B. R. 1994 Blooms of phytoplankton
including Emiliania huxleyi (Haptophyta). Effects of nutrient
supply in different N:P ratios. Sarsia 79, 333–348.
Guillard, R. R. L. 1978 Counting slides. In: Sournia, A. (ed.)
Phytoplankton Manual. Unesco, Paris, pp. 182–189.
Hasle, G. R. 1978 Using the inverted microscope. In: Sournia, A.
(ed.) Phytoplankton Manual. Unesco, Paris, pp. 191–196.
Hattori, H., Koike, M., Tachikawa, K., Saito, H. & Nagasawa, K.
2004 Spatial variability of living coccolithophore distribution
in the Western Subarctic Pacific and Western Bering Sea.
J. Oceanogr. 60, 505– 515.
Holligan, P. M., Groom, S. B. & Harbour, D. S. 1993 What controls
the distribution of the coccolithophore, Emiliania huxleyi,in
the North Sea? Fish. Oceanogr. 2, 175–183.
Jordan, R. W. & Chamberlain, A. H. L. 1997 Biodiversity among
haptophyte algae. Biodiv. Conserv. 6, 131–152.
Koray, T., Gokpinar, S., Polat, S., Turkoglu, M., Yurga, L., Colak,
F., Benli, H. A. & Sarihan, E. 2000 Comparison of the
qualitative characteristics of microplankton (protista) of
Turkish Seas (Black Sea, Aegean Sea, Northeastern
Mediterranean). EU. J. Fish. Aquat. Sci. 17(3–4), 231–247
(in Turkish).
Kormas, K. A., Garametsi, V. & Nicolaidou, A. 2002 Size-
fractionated phytoplankton chlorophyll in an Eastern
Mediterranean coastal system (Maliakos Gulf, Greece). Helgol.
Mar. Res. 56, 125–133.
Mikaelyan, A. S. 1997 Long-term variability of phytoplankton
communities in open Black Sea in relation to environmental
changes. In: Ozsoy, E. & Mikaelyan, A. (eds) Sensitivity to
Change: Black Sea, Baltic Sea and North Sea, NATO ASI
Series, (Vol. 27). Kluwer, Dordrecht, pp. 105–116.
Moncheva, S. & Krastev, A. 1997 Some aspects of phytoplankton
long-term alterations off Bulgarian Black Sea Shelf. In: Ozsoy,
E. & Mikaelyan, A. (eds) Sensitivity to Change: Black Sea,
Baltic Sea and North Sea, NATO ASI Series, (Vol. 27).
Kluwer, Dordrecht, pp. 79– 94.
Nanninga, H. J. & Tyrrell, T. 1996 The importance of light for the
formation of algal blooms by Emiliania huxleyi. Mar. Ecol.
Prog. Ser. 136, 195– 203.
Oguz, T. & Merico, A. 2006 Factors controlling the summer
Emiliania huxleyi bloom in the Black Sea: a modeling study.
J. Mar. Syst. 59, 173– 188.
Paasche, E. 2002 A review of the coccolithophorid Emiliania
huxleyi (Prymnesiophyceae), with particular reference to
growth, coccolith formation, and calcification-photosynthesis
interactions. Phycologia 40, 503 –529.
Piehler, M. F., Twomey, L. J., Hall, N. S. & Paerl, H. W. 2004
Impacts of inorganic nutrient enrichment on the
phytoplankton community structure and function
in Pamlico Sound, NC USA. Estuarine, Coast. Shelf Sci. 61,
197–207.
Polat, S. C. & Tugrul, S. 1995 Nutrient and organic carbon
exchanges between the Black and Marmara seas through the
Bosphorus strait. Cont. Shelf Res. 159, 1115–1132.
Polat, S. C., Tugrul, S., Coban, Y., Basturk, O. & Salihoglu, I. 1998
Elemental composition of seston and nutrient dynamics in the
Sea of Marmara. Hydrobiologie 363, 157–167.
Quinn, G. P. & Keough, M. J. 2002 Experimental Design and Data
Analysis for Biologists. Cambridge University Press, Cambridge.
Redfield, A. C., Ketchum, B. K. & Richards, F. A. 1963 The
influence of organisms on the composition of sea water. In:
Hill, M. (ed.) The Sea, (Vol. 2). Wiley, New York, pp. 26–77.
Roberts, E. C., Davidson, K. & Gilpin, L. C. 2003 Response of
temperate microplankton communities to N:Si ratio
perturbation. J. Plank. Res. 25, 1485 –1495.
Smyth, T. J., Tyrrell, T. & Tarrant, B. 2004 Time series of
coccolithophore activity in the Barents Sea, from twenty years
of satellite imagery. Geophys. Res. Lett. 31(11),
L11302.1–L11302.4.
Sorrosa, J. M., Satoh, M. & Shiraiwa, Y. 2005 Low temperature
stimulates cell enlargement and intracellular calcification of
coccolithophorids. Mar. Biotech. 7(2), 128 –133.
SPSS Advanced StatisticsY version 11.5 2003 SPS Inc., Chicago, IL.
113 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
Stefanson, U. & Richards, F. A. 1963 Processes contributing to the
nutrient distribution of Colombia River and the Strait of Juan
de Fuca. Limnol. Oceanogr. 8, 394 –410.
Strickland, J. D. H. & Parsons, T. R. 1972 A Practical Handbook of
Seawater Analysis, 2nd edition. Fisheries Research Board of
Canada, Ottowa, Canada.
Tekiroglu, S. E., Ediger, V., Yemeniciog
˘
lu, S., Kapur, S. & Akc¸a, E.
2001 The experimental analysis on the Late Quaternary
deposits of the Black Sea. Oceanol. Acta 24, 51–67.
Turkoglu, M. 2005 Succession of picoplankton (coccoid
cyanobacteria) in the Southern Black Sea (Sinop Bay, Turkey).
Pak. J. Biol. Sci. 8(9), 1318– 1326.
Turkoglu, M. 2008 Synchronous blooms of the coccolithophore
Emiliania huxleyi (Lohmann) Hay & Mohler and three
dinoflagellates in the Dardanelles (Turkish Straits System).
J. Mar. Biol. Assoc. UK 88(3), 433 –441.
Turkoglu, M. & Koray, T. 2000 Ecological and geographical
distributions of the planktonic protista in the southern part of
the Black sea (neritic waters of Sinop peninsula, Turkey). EU
J. Fish. Aquat. Sci. 17(1– 2), 161–178.
Turkoglu, M. & Koray, T. 2002 Phytoplankton species succession
and nutrients in Southern Black Sea (Bay of Sinop). Turk.
J. Bot. 26, 235–252.
Turkoglu, M. & Koray, T. 2004 Algal blooms in the surface waters
of the Sinop Bay in the Black Sea, Turkey. Pak. J. Biol. Sci. 7,
1577–1585.
Turkoglu, M. & Erdog
˘
an, Y. 2007a Daily and diurnal fluctuations of
summer phytoplankton, nutrient and chlorophyll-a in the
Dardanelles (C¸ anakkale Strait, Turkey). AfPR—Plankton
Symposium IV, Joao Pessoa, 1–5 April. BDUA J. Biol. 2,62
(abstract).
Turkoglu, M. & Erdogan, Y. 2007b Daily variation of summer
phytoplankton in the Dardanelles. Rapp. Comm. Int. Mer
Medit. 38, 399 (abstract).
Turkoglu, M., Buyukates, Y. & Kaya, S. 2004a Temporal
distribution of phytoplankton and nutrients in the
Dardanelles. Turk. J. Aquat. Sci. 2(3), 201 (abstract).
Turkoglu, M., Buyukates, Y. & Kaya, S. 2004b Excessive
blooms of coccolithophore Emiliania huxleyi and some
dinoflagellates in the Dardanelles. Turk. J. Aquat. Sci. 2(3),
423 (abstract).
Turkoglu, M., Unsal, M., Ismen, A., Mavili, S., Sever, T. M., Yenici,
E., Kaya, S. & Coker, T. 2004c Dinamics of lower and high
food chain of the Dardanelles and Saros Bay (North Aegean
Sea). TUBITAK Technical Final Report, 101Y081, 17100
C¸ anakkale, Turkey (in Turkish).
Turkoglu, M., Yenici, E., Ismen, A. & Kaya, S. 2004d Variations
of nutrient and chlorophyll-a in the Canakkale Strait
(Dardanelles). EU J. Fish. Aquat. Sci. 21(1–2), 93– 98
(in Turkish).
Turkoglu, M., Baba, A. & Ozcan, H. 2006 Determination and
evaluation of some physicochemical parameters in the
Dardanelles (Canakkale Strait—Turkey) using multiple probe
system and geographic information system. Nordic Hydrol.
37(3), 293–301.
Turkoglu, M., Buyukates, Y. & Oner, C. 2007 Short time variations
of winter phytoplankton, nutrient and chlorophyll-a in the
Dardanelles (C¸ anakkale Strait, Turkey). AfPR—Plankton
Symposium IV, Joao Pessoa, 1–5 April. BDUA J. Biol. 2,63
(abstract).
Tyrrell, T. & Taylor, A. H. 1995 A modelling study
of Emiliania huxleyi in the NE Atlantic. J. Mar. Syst. 9,
195–203.
Unsal, M., Turkoglu, M. & Yenici, E. 2003 Biological and
Physicochemical Researches in the Dardanelles. TUBITAK
Technical Research Report, 101Y075, 17100 C¸ anakkale,
Turkey (in Turkish).
Uysal, Z. 1995 A net plankton study in the Bosphorus junction of
the Sea of Marmara. Turk. J. Bot. 20, 321–327.
Venrick, E. L. 1978 How many cells to count? In: Sournia, A. (ed.)
Phytoplankton Manual. UNESCO, Paris, pp. 167–180.
Zeichen, M. M. & Robinson, I. S. 2004 Detection and monitoring
of algal blooms using SeaWiFS imagery. Int. J. Remote Sens.
25, 1389–1395.
First received 3 December 2008; accepted in revised form 15 September 2009. Available online February 2010
114 M. Turkoglu
|
Winter bloom of E. huxleyi and environmental conditions in the Dardanelles Hydrology Research
|
41.2
|
2010
