Coccolithophore biogeography in the South China Sea
In the context of the coccolithophore biogeographical zones of Winter et al.
(1994), the coccolithophore assemblages investigated in the SCS belong to
the tropical zone, comprising E. huxleyi, G. oceanica, Gephyrocapsa ericsonii, Oolithotus fragilis,
U. irregularis, F. profunda, and A. robusta.
Reticulofenestra sessilis was also sporadically found at 75 m depth
at sampling stations, and this species is reported to be exclusively found in
lower photic water of the tropical zone, where it may form symbioses
with diatoms (i.e., Thalassiosira species) (Winter et al., 1994;
Young et al., 2003; Jordan, 2012). The coccolithophore flora of the SCS is
similar to the “high temperature” and “warm oligotrophic” assemblages
in the equatorial Pacific Ocean (Hagino et al., 2000).
The two dominant species in our samples from the SCS were E. huxleyi
and F. profunda, species representative of the upper and lower
photic zone floral groups (Winter et al. 1994). These floral groups both live
within the euphotic zone (> 1 % surface irradiance), which is
about 100 m in summer in the SCS. However, in the western Pacific warm pool
(stratified waters) and subtropical gyres of the Pacific and Atlantic oceans,
species F. profunda are found much deeper (150 to 250 m) in the
water column (Hagino et al., 2000; Boeckel and Baumann, 2008; Beaufort et
al., 2008). These differences are undoubtedly linked to differences between
the SCS and open ocean in terms of the depths of the thermocline and nutricline,
implying that the SCS is relatively eutrophic when compared with tropical and
subtropical settings at a similar latitude.
Upper photic zone (UPZ) assemblage
In our nMDS analysis, the UPZ
assemblage (Winter et al., 1994) was represented by Groups 1 and 2, found at
25 and 50 m in the SCS. These two groups have different species composition
in our analysis; for example, Group 1 included umbelliform species, i.e.,
U. irregularis, which are considered K selected (specialist)
species (Young, 1994), and this agrees with previous work (e.g., Okada and
Honjo, 1975). The UPZ assemblage is commonly observed in well-stratified,
oligotrophic, warm surface waters in the western Pacific warm pool (Hagino et
al., 2000). In the SCS, U. irregularis was mostly found at stations
with deep mixed layers, deep nutriclines, and extremely low nutrients in
surface waters. In comparison, Group 2 occurred at stations with shallower
mixed layers and nutriclines and hence potentially elevated nutrient
supplies, and coccolithophores in this group were most abundant and diverse,
which indicates that this community was slightly productive when compared
with those in other groups. The E. huxleyi dominance contradicts
other studies in the SCS in summer, such as Okada and Honjo (1975) and Sun et
al. (2011), who found that G. oceanica was the dominant species (30
to 100 % of total cell numbers) in the western and southern parts of the
SCS. Differences between this study and others could relate to the influence
of the Asian summer monsoon on the western and southern SCS, where the
southwesterly wind causes a wind-driven upwelling system off the east coast
of Vietnam (Liu et al., 2002; Xie et al., 2003; Ning et al., 2004).
G. oceanica is considered a more eutrophic and coastal species
(Andruleit and Rogalla, 2002; Andruleit et al., 2003), and hence it
contributed less to coccolithophore cells in the central and northern part of
SCS, where summer-monsoon-induced upwelling or water mixing is weak.
The relative contribution of E. huxleyi + G. oceanica and F. profunda to coccolithophore-based calcite
concentration in the water column at all stations (a); at I1, I2, I3, I4,
I5, and H3 (b); and at X3, X4, I6, I7, F1, and D9 (c). The solid lines
denote moving average of 30 grid points. (d) Yearly averaged
coccolith relative abundance and their contribution to coccolith-based
calcite in sediment trap (117.46∘ E 20∘ N, 500 m) in the
South China Sea (Jin et al., unpublished).
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Pearson's product-moment correlations (r) between mean distal
shield length (DSL) of E. huxleyi, principal component 1 (PC-1)
scores and environmental parameters: nitrate + nitrite (N), phosphate
(P), pH, total alkalinity (AT), CaCO3 saturation
(ΩC), and temperature (T) (n=29). The principal component
analysis is based on all the environmental parameters, with a PC-1
contribution of 76.59 % to total variance. * p< 0.05; **
p< 0.01.
Mean DSL
PC-1 (76.59 %)
N
0.601**
-0.967**
P
0.579**
-0.965**
pH
-0.526**
0.804**
AT
0.274
-0.671**
ΩC
-0.395*
0.958**
T
-0.21
0.842**
Morphotype A was the dominant morphotype of E. huxleyi in the SCS.
Different morphotypes of E. huxleyi can be distinguished by
coccolith characteristics such as DSL, element widths, and features of the
central area (e.g., Young et al., 2003; Hagino et al., 2011) and may be
considered different ecotypes with different temperature and nutrient
preferences (Cook et al., 2011; Poulton et al., 2011; Hagino et al., 2011;
Saavedra-Pellitero et al., 2014). In general, E. huxleyi type A
shows a warmer-water preference than type B and other type B derivatives (C,
B/C). In our observations, type C E. huxleyi coccospheres or coccoliths
were only found sporadically in SEM images, and the predominant occurrences
of morphotype A could be related to the prevailing high sea-surface
temperature (> 26 ∘C) in the study area. The southern
part of SCS is also within the western Pacific warm pool, where sea-surface temperature is consistently > 28 ∘C
all year round (Yan et al., 1992).
Lower photic zone (LPZ) assemblage
In the present study, the LPZ was
represented by Group 3, which included typical LPZ species (F. profunda, A. robusta, and G. flabellatus) and was found
between 75 and 100 m. Group 3 occurred above, at, or near the depth where
1 % of surface irradiance penetrated (i.e., base of the euphotic zone).
In other tropical oceans, the LPZ assemblage dwells deeper than the base of
the euphotic zone (Hagino et al., 2000; Boeckel and Baumann, 2008; Beaufort
et al., 2008). In the northern Arabian Sea, F. profunda inhabits
shallower waters and is found across a wider depth range (10 to 80 m)
(Andruleit et al., 2003). It is worth noting that, as in the SCS, the Arabian
Sea is strongly controlled by a monsoonal system (Indian monsoon) and is
considered relatively eutrophic (Andruleit and Rogalla, 2002; Andruleit et
al., 2003). Hence, it can be inferred that neither water depth nor light
availability is a limiting factor for F. profunda (and/or other LPZ
species) in the SCS, but rather nutrient availability is important; the
nutricline is relatively shallow (50 to 75 m) even in the oligotrophic
summer in the SCS.
The response of coccolithophores to eddies in the South China
Sea
Mesoscale eddies have a strong influence on productivity and ecosystem
structure in the SCS (Chen et al., 2007b; Lin et al., 2010; Wang et al.,
2016). Previous measurements in the SCS have shown that integrated primary
production in cyclonic eddies can be 2–3-fold higher relative to the outside
of eddies (Chen et al., 2007b). Modeling results have also highlighted how
new production can be ∼ 30 % higher
or lower, relative to outside of eddies, in cyclonic or anticyclonic eddies, respectively (Xiu and Chai,
2011).
Results from nMDS, HCA, and eddy settings in the 18∘ N section
clearly show that the coccolithophore communities in the SCS were strongly
coupled with eddy occurrences (Fig. 5). In the cyclonic eddy (I3, H3),
Group 2 occurred in ranges of 25 to 50 m depth and Group 3 occurred within
layers from 75 to 100 m. Comparatively, at stations (X5, G2) with “normal”
(non-eddy) conditions, three groups sequentially occurred in the
water column: Group 1 at 25 m, Group 2 at 50 m, and Group 3 between 75 and 100 m depth. In anticyclonic eddies, there were two patterns: one with
Group 1 distributed within a wider depth range (from 25 to 50 m) and
Group 3 only within a 100 m layer; the other was that Group 2 was absent,
and the maximum coccolithophore abundance depth was deep and belonged to
Group 3, which was dominated by LPZ assemblages (e.g., F. profunda).
This variation highlights the importance of the ecological effects of eddies on
the coccolithophore community's depth distribution through the water column.
As the anticyclonic eddy (cyclonic eddy) centers lead to convergence
(divergence) of the adjacent waters, they deepen (shoaling) the nutricline and
creating more oligotrophic (slightly eutrophic) conditions in the water
column which favor distinct coccolithophore assemblages (Fig. 8).
Schematic showing the coccolithophore communities in an anticyclonic
eddy and a cyclonic eddy.
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E. huxleyi distal shield length plot versus coccosphere
diameter (a) in the present study with comparison with those from
other field and culturing samples (Triantaphyllou et al., 2010; Henderiks et
al., 2012; Bach et al., 2012; Müller et al., 2012). These E. huxleyi biometry data are derived from Fig. 6 in Müller et al. (2012).
(b) Scatterplot of single coccolith weight (calculated from Eq. 2)
and number of coccoliths per coccosphere (N), showing the particulate
inorganic carbon (PIC) per cell.
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Due the discontinuous sampling dates (Table 1) and low resolution of
environmental data at some stations, the meridional section may not be
suitable for assessing the eddy impacts on coccolithophore communities. For
example, at I6 and I7, stations were not characteristic of anticyclonic
eddies based on the SLA and geostrophic flow map; however, the
coccolithophore community vertical composition or structure is similar to those
in the anticyclonic eddies. This may be due to the deeper nutricline in the
central basin of the SCS, even if the water-column structure had not been
modulated by eddies in our investigation. Another example is stations I1 and
I2, for which the coccolithophore groups agreed with those in the cyclonic
eddies. Likewise, this was also not characteristic of the cyclonic eddies, as
shown by SLA and geostrophic flow (Supplement). At stations I1 and I2, the
euphotic zone depth was relatively shallow (∼ 70 m), with more light
attenuation from suspended particles, which could be caused by elevated
particle production. This finding corresponds to the station locations at
the edge of the anticyclonic eddy where particulate organic carbon (POC)
fluxes can be 2–4-fold higher than those in adjacent oligotrophic waters
(Zhou et al., 2013; Shih et al., 2015). For station I4, the case was similar
to I1 and I2, as it was located at the edge of two large anticyclonic eddies
(supplement). The horizontal advection, for water mass balance, can result in
the elevated nutricline in anticyclonic eddy edges and, hence, the
enhancement of POC production and export (Zhou et al., 2013).
Station I5 had another distinctive arrangement of species assemblages, which
was the opposite of that found at the other stations sampled (Fig. 5); Group 2
was found at 25 m while Group 1 was at 50 m. Examination of the temperature
profile shows that the 29.5 ∘C isotherm was shallow and domed, while
the 22.5 ∘C isotherm was pushed deeper into the water column
(Fig. 2b). Filters collected at 25 and 50 m from I5 also had lots of diatom
fragments and relatively elevated coccolithophore abundances (21.75 and
22.59 cells mL-1 at 25 and 50 m, respectively). We suggest that this
feature may represent a mode-water eddy, as described by McGillicuddy et
al. (2007) in the northeast subtropical Atlantic Ocean. McGillicuddy et
al. (2007) observed elevated phytoplankton production (i.e., a diatom bloom)
in a mode-water eddy, which led to local changes in the zooplankton community
composition (McGillicuddy et al., 2007; Eden et al., 2009).
Calcite concentrations in the South China Sea
The discrete estimates of bulk coccolith calcite roughly covaried with
coccolith and coccolithophore concentration in the water column, with peak
concentrations around the DCM. Excluding the maximum calcite concentration in
the DCM, another peak was also found in deeper water at some stations, for
example at 150 m in F1 and D9 and 100 and 150 m in I7, where the cell
concentrations were low and calcite was nearly entirely contributed by detached
coccoliths. In addition, the relative calcite contribution of different taxa
changed in different trophic levels of the water column. For example, the
relative calcite contribution of the common placolith (i.e., G. oceanica and E. huxleyi) was higher in the water column with slightly
euphotic stations (e.g., stations with cyclonic eddy, shallow DCM, and
nutricline; Fig. 3). Their contribution decreased and the contribution of
F. profunda increased with the deepening of water depth, whereas the
contribution of other species remained constant (Fig. 7b). In contrast, these
placoliths contributed less in water columns with an oligotrophic station (e.g., stations with anticyclonic eddy, deep DCM, and nutricline; Fig. 3),
and an elevated contribution of other species was found in the upper ∼ 50 m of the water column (Fig. 7c). E. huxleyi, G. oceanica, and
F. profunda represented around half of the calcite in the water
column, whereas other species with smaller levels of abundance contribute to
the other 50 % of water-column calcite. The greater contribution of these
relatively less abundant species in calcite inventories is partly related to
higher per coccolith calcite contents, due in part to larger coccolith
lengths (Young and Ziveri, 2000); for example, O. fragilis has
> 80 pg C per coccolith, whereas E. huxleyi has
∼ 2 pg C per coccolith. Relatively rare coccolithophore species with
high coccolith and coccosphere calcite contents are important vectors of both
upper-ocean calcite production (Daniels et al., 2014) and deep-sea calcite
fluxes (Ziveri et al., 2007). However, an examination of sediment trap material
(500 m depth, 1500 m above the sea floor) in the northern SCS basin shows
that these three species (E. huxleyi, G. oceanica, and
F. profunda) dominating upper-ocean calcite inventories all have an
increased contribution to coccolith (> 95 %) and coccolith
calcite (> 80 %) fluxes (Fig. 7d, Jin et al., unpublished). The
significant loss of the calcite contribution from other species highlights
the discrepancy between coccolith calcite in the euphotic upper water column
and aphotic deep ocean. Notably, at 150 m for some stations (D9, F1, G2, I5,
X3), these three species can comprise more than 70 to 90 % of calcite
inventories and the contribution of G. oceanica exceeds that of
E. huxleyi, which is similar to the fluxes of sediments of moored
traps. One possible reason is that these coccoliths are attributed to lateral
transport of the nepheloid layer originating from the continental shelf or slope.
This is the most likely case for D9 and F1, as they have such high
detached coccolith concentrations (Fig. 6) and are located in the easternmost
part of the 18∘ N section. Alternatively, coccoliths in the deep layer
are a result of vertical sinking. They can indicate that the higher
contribution of these species in the deep layer may result from their higher
production rate in the photic zone, which cannot be reflected by the
snapshot-like discrete sampling done in our study.
(a) Cell abundance (red triangles) and mean distal shield
length (DSL, blue dots; error bar: 1 SD) of E. huxleyi plotted
at stations where there were at least two biometry measurement points.
(b) A schematic map showing light and nutrient conditions in
relation to coccolithophore growth rate and cell or coccolith size.
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Environmental influences on <italic>Emiliania huxleyi</italic> biometry
Some parameters can describe coccolithophore calcification in field or
culturing studies. Firstly, coccolith biometry, which includes the parameters
of coccolith morphology such as shield length, thickness, and relative tube width (e.g., Poulton et al., 2011; Young and Ziveri, 2000; Young et al., 2014), is
directly associated with single-coccolith weight or calcite content. Our data
indicate that the biometry parameters of the E. huxleyi coccosphere,
i.e., CD, DSL, and N, are significantly correlated (results 3.4). The linear
relationship between DSL and CD (morphotype A cells) was also reported in
field (Triantaphyllou et al., 2010; Henderiks et al., 2012) and culture
samples (Bach et al., 2012; Müller et al., 2012) (Fig. 9a). As suggested
by Müller et al. (2012), it takes additional time for larger-sized cells
to transport coccoliths from vesicle to cell surface and hence more time for
coccolith maturation and formation so as to produce a larger-sized coccolith.
By multiplying single-coccolith weight by the number of coccoliths per coccosphere, we
get the cell calcite content, which mainly ranges from 10 to 70 pg for an
E. huxleyi type A cell in the SCS (Fig. 9b). The DSL / CD ratios for
E. huxleyi type A in the culturing and field samples are both within
their respective ranges, and the former is obviously higher than the latter
(Fig. 9a), which can be attributed to the fact that changes in a sole environmental
variant in sterile culture experiments can remarkably influence the
physiology of coccolith formation, whereas the effects on coccolith formation
can be muted due to the positive or negative responses to multiple
environmental changes in the field (Müller et al., 2012). With the same DSL,
coccosphere diameter in field samples is larger. It also seems that an E. huxleyi cell in the field can produce more or multilayer coccoliths, which could be a defense against zooplankton grazing or
bacterial attack and offer mechanical protection (Young, 1994; Jaya et al.,
2016) in natural conditions. As seen in Fig. 9b, the coccolith length
is likely to be able to reflect the morphology of a whole coccosphere and its
calcite content, i.e., the cellular particulate inorganic carbon (PIC)
content. And further, the linear relationship between the morphological
parameters makes it possible to reconstruct coccolithophore cell volume in
geological records (Henderiks, 2008).
The second parameter is PIC production rate, i.e., the calcification rate, which
is calculated by the equation PPIC= growth rate
(μ) × cellular PIC content in batch cultures (e.g., Langer et
al., 2006, 2009, 2012). Another is cell-specific calcite production (CP)
(e.g., Poulton et al., 2013, 2014; Charalampopoulou et al., 2011, 2016), which
is calculated by dividing CP by cell abundance. These two parameters are
obviously related to the cellular PIC content or single-coccolith calcite
content; however, they are not equivalent because both calcification rate and
cell-specific CP are also strongly influenced by coccolithophore or the coccolith
production rate. Hence, the following discussion is based on the coccolith
biometry-related parameters, e.g., coccolith or coccosphere length,
coccolith or coccosphere calcite content (weight).
Nutrient and light
The statistically significant correlation between the nutrient and mean DSL
of E. huxleyi suggests that both nitrogen and phosphorus exert a positive
influence on coccolith length. However, in nutrient-limited batch cultures,
it has been shown that E. huxleyi morphology displayed divergent
responses to different types of resource limitation; e.g., coccolith or
coccosphere length or volume and/or calcite content deceased and increased
under nitrogen- and phosphorus-limited conditions, respectively (Riegman et
al., 2000; Müller et al., 2008, 2012; Oviedo et al., 2014). The increased
coccolith or coccosphere size of E. huxleyi was also found in
phosphorus-deficient mesocosm enclosures (Båtvik et al., 1997; Engel et
al., 2005). The interpretation is that nitrogen and phosphorus are required
for distinctly different cellular uses: nitrogen for biomass growth and
phosphorus for cell division and organic maturity (e.g., Arrigo, 2005;
Aloisi, 2015). Therefore, under nitrogen limitation, coccolithophores will
produce smaller cells with a smaller-sized coccolith, and on the other hand,
phosphorus limitation inhibits cell division, whereas biomass in cells still
grows, leading to an increase in coccolith or coccosphere size (Müller et
al., 2008, 2012). Back to the present case, the nutrient limitation theory
indicates that nitrogen should be the main controlling factor on coccolith
size. The positive relation of DSL and phosphorus may come from the high
intercorrelation between the two types of nutrients (Pearson, r = 0.99,
p< 0.01).
E. huxleyi type A distal shield length (DSL) in the South
China Sea (black circles) with those in neritic populations (hollow diamonds) and
oceanic populations (hollow triangles) in the North Sea (Young et al., 2014), plotted versus
carbonate calcium saturation (ΩC).
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Nutrient is an important limiting factor in E. huxleyi growth (i.e.,
under laboratory culturing conditions); when nutrients are replete, E. huxleyi growth is fast (exponential phase), with fewer and smaller
coccoliths per cell. When nutrients become limiting, E. huxleyi
growth slows (stationary phase), and larger and multilayer coccospheres are
produced (Gibbs et al., 2013). Besides nutrients, it is suggested that light
should also be a limiting factor for E. huxleyi production and
calcification in natural community (e.g., Poulton et al., 2007, 2010, 2014;
Charalampopoulou et al., 2011). With a closer inspection of the DSL data, the
largest coccoliths occurred at the deepest depths where nutrients were sufficient and light was insufficient, while within the E. huxleyi
abundant depth coccoliths were relatively small (most remarkable at X3, F1,
D9, I7, X5; Fig. 10a). Estimated from the monthly (June 2014) instantaneous
PAR (∼ 2000 µmol m-2 s-1, ocean color Aqua-MODIS
satellite) in the SCS, the PAR in the water column was about 200, < 100, and
20 µmol m-2 s-1 at 50 (10 %), 75
(< 5 %), and 100 m (1 %) depth, respectively. E. huxleyi growth is likely to be limited by light, although some authors have
stated that light should not be regarded as a factor regulating phytoplankton
growth in the oligotrophic SCS as the euphotic zone depth exceeds the MLD and
nutricline throughout the year (Tseng et al., 2005; Wong et al., 2007). The
higher half-saturation constants of E. huxleyi for light
(∼ 100 µmol m-2 s-1 for E. huxleyi and
∼ 40 µmol m-2 s-1 for other phytoplankton groups; Tyrrell and Taylor, 1996) may support our statement that E. huxleyi
growth is more light-dependent in the SCS. Here, we propose a simple
schematic (Fig. 10b). (1) In the DCM layer, where light and nutrients are
optimal for phytoplankton growth, E. huxleyi growth is fast and the species produces small-sized coccoliths. (2) In deeper waters, when nutrients are more
sufficient but light is not available, E. huxleyi growth slows and
the species produces larger-sized coccoliths. It has been reported that an E. huxleyi cell can produce higher-calcite-content coccoliths with a lower growth
rate in light-limited continuous cultures (Fritz and Balch, 1996; Fritz,
1999). That light limitation, in E. huxleyi cells, can prolong the G1
assimilation stage during which calcification takes place and will eventually increase cellular calcite content (Müller et al., 2008). Although
coccolith formation is a light-dependent process, it does not seem to be
impeded in the low-light conditions. This could be owing to the calcification having a lower light-saturated threshold than photosynthesis
(Müller et al., 2008). (3) Above the nutricline, where light intensity is
high and multi-nutrients are depleted, it is possible that E. huxleyi coccolith size is dependent on whether inorganic phosphorus is
deficient or organic phosphorus compounds can be utilized, although we lack
data to directly address either nutrient availability or coccolith biometry
in these samples.
Temperature
Temperature is expected to be a critical factor for coccolithophore growth and cell
size. An E. huxleyi strain isolated from Great Barrier Reef showed
an optimal growth temperature at 25 ∘C with the smallest cell size,
while the growth rate and cell size became lower and bigger in parallel as the
temperature was decreased to 10 ∘C (Sorrosa et al., 2005). A recent
culturing study (Saruwatari et al., 2016) has also shown that E. huxleyi strains of the morphotype B/C isolated from the Arctic Ocean grow faster
and produce smaller coccoliths when temperature increases from 5 to
20 ∘C. However, contradictory results come from Rosas-Navarro et
al. (2016), who have found that E. huxleyi (type A, strains isolated
from North Pacific Ocean) produces the largest coccoliths within the optimal
growth temperature of 20 to 25 ∘C. Apparently, these different
patterns of E. huxleyi coccolith size may result from
strain-specific or morphotype (ecotype) responses to temperature. In the
present study, temperature was not found to correlate with E. huxleyi coccolith size from the statistical analysis (Table 3). One possible
reason could be that the temperature profiles were to a large extent controlled
by the eddy-related water-column structure (i.e., MLD), which may possibly
mute the signal of their influences on E. huxleyi growth and size.
Alternatively, as stated by Bach et al. (2012), temperature may exert little
physiological influence on E. huxleyi size. In addition, the
temperature at the investigated stations ranged from 18 to 25 ∘C at
depths from 100 to 50 m, which is near the optimal growth temperature for
many E. huxleyi strains (20 to 25 ∘C; Paasche, 2002;
Sorrosa et al., 2005; Rosas-Navarro et al., 2016). That is, temperature may
not be a limiting factor for E. huxleyi growth within the euphotic
zone in the tropical SCS, apart from surface and/or near-surface waters where
water temperatures are > 29 ∘C, above the growth optimum
temperature range for this species (Rosas-Navarro et al., 2016).
Carbonate chemistry
Coccolithophores are thought to be sensitive indicators of carbonate
chemistry, especially ΩC and [CO32-] (e.g., Beaufort
et al., 2011). Our results show that the mean DSL is inversely correlated
with pH and ΩC. Indeed, all the environmental data were
significantly intercorrelated (Table 3), nearly all contributing to one
principal component (PC-1, 76.59 % of variance) (Table 3). That is, the
environmental gradients in the water column are dependent on sampling depth.
Importantly, in the data from the SCS the carbonate chemistry inversely
mirrors the nutrient data, making it hard to distinguish its influence on
coccolith morphology. Similarly, due to the high intercorrelation levels of
all environmental variants in two transects in the Southern Ocean, carbonate
chemistry does not seem to be the best interpretation for E. huxleyi
cell-specific calcification (Charalampopoulou et al., 2016). Hence, it is not
possible to directly infer that E. huxleyi coccolith size and
carbonate chemistry have a simple cause and effect relationship in the SCS.
Here, our DSL results in the SCS were compared with those in the North Sea
(Young et al., 2014) (Fig. 11). In the North Sea, E. huxleyi was
also dominated by morphotype A (Young et al., 2014). While
ΩC in the two regions falls within a similar range, DSL
shows a significant difference (F = 17.18, p< 0.01). Young
et al. (2014) have argued that E. huxleyi DSL differences relate to
neritic and oceanic groups rather than to carbonate chemistry impacts. DSLs in
our samples show no significant difference with those in the oceanic group
(F = 0.243, p = 0.63); however, they are significantly lower than
those in the neritic group from Young et al. (2014) (F = 125.2, p< 0.01) (Fig. 11). Hence, what causes the morphological distinction
may be genotypic variation or an ecological effect (Bach et al.,
2012). It is suggested that the changing environmental conditions can select
for different coccolithophore strains, which indirectly influences the
coccolith size and morphology (Bach et al., 2012). For example, different
environmental provinces can shift from a community dominated by normally
calcified E. huxleyi type A to one characterized by weakly calcified
B/C on the Patagonian Shelf and in the Southern Ocean (Cubillos et al., 2007;
Poulton et al., 2011). More heavily calcified morphotypes during low
ΩC in winter may be responsible for the seasonal morphotype
transition in the Bay of Biscay (Smith et al., 2012). Seasonal variability of
E. huxleyi coccolith size has also been observed in the Aegean Sea,
which may be due to genotypic or ecophenotypic variation (Triantaphyllou et
al., 2010). Meier et al. (2014) found that mean coccolith weight peaked at
the Rockall Plateau during Heinrich event 11, when ΩC and pH
had minimum values. This could be due to a coccolith assemblage shift to
more heavily calcified morphotypes in relation to oceanic frontal changes during
this geological episode rather than the influences of carbonate chemistry
(Meier et al., 2014). In conclusion, the ecological transition of assemblages
may have a more dominant effect on coccolith morphology and/or cellular
calcification not only in the present ocean but also in geological records.