Introduction
Coccolithophores are a group of calcifying unicellular phytoplankton within
the Prymnesiophyceae (Paasche, 2002). They are an ecologically and
biogeochemically prominent marine phytoplankton functional group, and
contribute to carbon dioxide (CO2) sinks and sources by performing both
photosynthesis and calcification, respectively (Raitsos et al., 2006; Raven
and Crawfurd, 2012). Although the ballasting of photosynthetic products by
coccoliths helps to efficiently transport carbon from the photic zone, the
calcification process is a net source of CO2 to the environment (Rost
and Riebesell, 2004; Gattuso et al., 1996). Therefore, the ratio of
photosynthesis to calcification determines their net contribution to
CO2 uptake or release. Consequently, investigating changes in these two
processes under varying environmental conditions is a key to our
understanding of their biogeochemical roles under ocean global change.
Calcification and photosynthesis of coccolithophores are influenced by many
factors, including nutrients, light availability, and CO2, as well as
temperature and ultraviolet radiation (UVR) (Riebesell et al., 2017; Tong et
al., 2016; Feng et al., 2008).
The rising atmospheric CO2 concentration due to human activities causes
greenhouse warming of the atmosphere and ocean, and the dissolution of this
anthropogenic CO2 into the surface ocean reduces the pH of seawater
in a process known as ocean acidification (OA). Previous studies have predicted that ongoing OA
will decrease the pH by 0.40 units in pelagic waters (Gattuso et al., 2015) and by
0.45 units in coastal waters (Cai et al., 2011) by the end of this century
under the business-as-usual CO2 emissions scenario. Conversely,
increased atmospheric CO2, along with other greenhouse gases,
will warm the Earth's surface by 2.5–6.4 ∘C by the year 2100
(Alexiadis, 2007), while the surface ocean temperature is projected to rise
by 2–3 ∘C (Stocker et al., 2014). Most previous work has indicated
that warming enhances stratification (Capotondi et al., 2012), although this has
recently been disputed (Somavilla et al., 2017). Assuming that ocean warming
is shoaling the depth of the upper mixed layer (UML), this would affect the
integrated levels of photosynthetically active radiation (PAR) and
UVR to which phytoplankton cells within the UML are
exposed (Häder and Gao, 2015). Regardless, increasing concentrations of
CO2 and other greenhouse gases will also begin to play an
ever-increasing role in determining levels of cloud cover and stratospheric
ozone, thus affecting the amount of UVR reaching ocean surface (Williamson et
al., 2014).
All of these ocean global changes may have individual and/or interactive effects
on the physiology of marine primary producers (Hutchins and Fu, 2017; Gao et
al., 2012). OA usually decreases the calcification of E. huxleyi,
although corresponding pCO2 increases can enhance
photosynthesis or growth at the same time (Riebesell et al., 2017, 2000).
Under nutrient replete conditions, increased light levels appear to
counteract the negative impacts of OA on the calcification of E. huxleyi
(Jin et al., 2017). The calcified coccoliths are thought to play roles in
protection against grazing pressure, viral and bacterial attack (Monteiro et
al., 2016), and can also help protect cells from UV radiation (Gao et al.,
2009). Early experiments on E. huxleyi strain BT-6 showed that cells
had a complete covering of coccoliths at 12.5–23 ∘C, but at
26.5 ∘C, 30 % of the cells had an incomplete covering (Paasche,
1968). Similarly, Langer et al. (2009) saw an increased occurrence of malformed coccoliths in
E. huxleyi RCC 1238 at 25 ∘C compared with those grown at 20
and 10 ∘C . A recent study showed that increased temperature
aggravates the impacts of OA on E. huxleyi morphology (Milner et
al., 2016).
Increasing levels of PAR or temperature and changes in UVR and nutrient
availability may interact with each other to cause additive, antagonistic or
synergistic effects for coccolithophores. Nevertheless, most previous studies
have been carried out under PAR only conditions, with UVR or fluctuating solar
radiation not being considered. However, UVR cannot be ignored when examining the
effects of environmental changes on marine phytoplankton that are found in
the upper half of the euphotic zone, as UV irradiance can penetrate as
deep as 80 m in pelagic waters (Tedetti et al., 2007). Excessive solar UV-B
and UV-A can damage DNA and interfere with many cellular biochemical
processes (Häder et al., 2014). Conversely, moderate levels of UVA
can enhance photosynthetic carbon fixation of phytoplankton assemblages (Gao
et al., 2007; Helbling et al., 2003). As for UVR effects on coccolithophore
calcification, recent studies have demonstrated that the outer coccoliths of
E. huxleyi can effectively shield the cells from a certain
percentage of UVR radiation (Xu et al., 2016). Nevertheless, the transmitted
energy still causes a significant inhibition of calcification, as well as
photosynthesis (Gao et al., 2009). The exposure of E. huxleyi to solar
UV radiation has been found to decrease its growth rate, but increase its production of
coccoliths per cell (Guan and Gao, 2009).
As exposure to solar UV radiation can influence cytoplasmic redox
activities (Wu et al., 2010), and inhibit or enhance physiological
performances at different levels of UVR, we hypothesized that the effects of OA
and warming on coccolithophores would be different with and without the
presence of UVR. To test our hypothesis, in this study we examined the
responses of E. huxleyi photosynthesis and calcification to OA with
or without UVR at three temperature levels.
Results
Thermal reaction norms
The growth temperature curve (growth thermal norms) obtained for E. huxleyi (Fig. 1) exhibited different shapes for the LC and the HC-grown
cells. The LC cultures showed an asymmetric pattern that is common to many
algal species, in which the growth rate increased with rise in temperature to
reach a maximum of 1.3 d-1 at 22.2 ∘C and then declined
sharply at temperatures above this optimal point (Table 2). At 20 and 24 ∘C,
the growth rate was <10 % lower than at 22.2 ∘C; therefore, 20 and
24 ∘C were still within the optimal growth temperature range for
LC-grown E. huxleyi. The HC-grown cells showed a relatively
symmetric thermal norm, with an optimal growth temperature of
20.6 ∘C, 1.6 ∘C lower than that of the LC-grown cells. Thus
the growth rate at 20 ∘C was near maximal, while the value at
24 ∘C decreased by nearly 20 % compared with the maximal growth
rate. The net effect of these trends was that the growth rate of the LC-grown
cells was significantly (p<0.05) higher than that of the HC-grown cells at
22 and 24 ∘C (Fig. 1).
Specific growth rate of E. huxleyi grown in
400 µatm (LC) and 1000 µatm (HC) CO2
concentrations at 15, 20 and 24 ∘C, respectively. The different
letters above the bars indicate significant differences among the treatments
(p<0.05). The values are the means, and the error bars are standard
deviations for triplicate cultures for each treatment.
Growth rate
During the 10 generations of growth at two CO2 levels and three
temperatures prior to the UV exposure, the growth rate was lowest at
15 ∘C and was further reduced by 17.4 % in HC-grown cells
compared with LC-grown cells (p<0.05, Fig. 2). At 20 ∘C, there was
no difference in growth rates between the HC- and LC-grown cells (p>0.05). At
24 ∘C, the growth rate did not change in LC-grown cells (p>0.05), but
decreased in HC-grown cells compared to that at 20 ∘C; thus, the
growth rate was 17.5 % lower in HC-grown cells compared with LC-grown cells at
24 ∘C (p>0.05).
The cellular POC (a), cellular PIC (b), POC production
rate (c), PIC production rate (d), inner coccosphere
volume (e) and PIC / POC ratio (f) of E. huxleyi grown in 400 µatm (LC) and 1000 µatm (HC)
CO2 concentrations at 15, 20 and 24 ∘C, respectively. The
different letters above the bars indicate significant differences among the
treatments (p<0.05). The values are the means, and the error bars are
standard deviations for triplicate cultures for each treatment.
Cellular PIC and POC quotas, production rates and inner coccosphere
volumes
The two CO2 treatments had no effect on cellular POC content at 15
and 20 ∘C. However, at 24 ∘C, the HC treatment
significantly increased cellular POC by 18.4 % compared with the LC
treatment (p<0.01, Fig. 3a), yielding the highest value among the
treatments. Cellular PIC content was reduced with increased CO2
concentration in the 15, 20 and 24 ∘C treatments by 35.8 % (p<0.05, Fig. 3b), 62.6 % (p<0.05) and 17.1 % (p<0.01),
respectively. In LC-grown cells, cellular PIC was significantly affected by
temperature, with the highest values observed at 15 ∘C, a decrease
of 34.2 % (p<0.01) at 20 ∘C and a decrease 18.9 % (p<0.01) at
24 ∘C. In HC-grown cells, cellular PIC was 45.2 % (p<0.01)
and 41.7 % (p<0.01) lower at 20 ∘C, compared with that at 15 and
24 ∘C, respectively. The production rate of POC ranged from 6.8 to
13.2 pg cell-1 d-1 among different treatments (Fig. 3c). At
15 ∘C, the HC treatment reduced the POC production rate by 26.6 %
(p<0.05), and the values were 42 % (p<0.01) and 30 % (p<0.01) lower in HC- and LC-grown cells, respectively, compared with those at
20 ∘C. No significant differences were observed between different
CO2 treatments at 20 and 24 ∘C (p>0.05), and the
temperature rising from 20 to 24 ∘C also had no significant effect
on the POC production rate in either HC- or LC-grown cells (p>0.05). The HC
treatment lowered the PIC production rate by 42.3 % (p<0.01, Fig. 3d),
37.3 % (p<0.01) and 29.9 % (p<0.01) at 15, 20 and
24 ∘C, respectively. A 5 ∘C temperature decrease from
20 ∘C had no significant effect on the PIC production rate in either the LC-cultures
or the HC-cultures (p>0.05). However, a 4 ∘C increase from 20 to
24 ∘C enhanced the PIC production rate by 41.9 % (p<0.05) and
27.4 % (p<0.05) in HC- and LC-grown cells, respectively.
The cellular PON content (a) and C / N ratio (b)
of E. huxleyi grown in 400 µatm (LC) and
1000 µatm (HC) CO2 concentrations at 15, 20 and
24 ∘C, respectively. The different letters above the bars indicate
significant differences among the treatments (p<0.05). The values are the
means, and the error bars are standard deviations for triplicate cultures for
each treatment.
Photosynthetic carbon fixation rates (a–c) under P
(irradiances above 395 nm), PA (irradiances above 320 nm) and PAB
(irradiances above 295 nm), and inhibition of photosynthetic carbon fixation
rates (d–f) due to UVA, UVB and UVR of E. huxleyi in HC-
and LC-grown cells at 15, 20 and 25 ∘C . Lines above the histogram
bars indicate significant differences between the HC and LC treatments, and
the different letters indicate significant differences among the radiation
treatments within the HC- or LC-grown cells within each panel.
The pattern of inner coccosphere volume among different treatments was
similar to that of cellular POC (Fig. 3e), with a significantly higher value
in HC-cultures than in LC-cultures at 24 ∘C (p<0.01), while no
difference existed between different CO2 treatments at the other
temperature levels (p>0.05).
The PIC to POC ratio (PIC / POC) had the lowest value at 20 ∘C
in the HC treatment (Fig. 3f), and the highest value at 15 ∘C in the
LC treatment. Either reduced or elevated temperature from 20 ∘C
increased the PIC / POC ratio in both HC- and LC-cultures (p<0.05),
although the extent varied.
Cellular PON content and POC / PON (C / N) ratio
Cellular PON displayed the same trends between the HC and LC treatments at 15 and
20 ∘C (p>0.05, Fig. 4a). Similar to cellular POC, at
24 ∘C cellular PON was 29.6 % higher in HC-grown cells compared
with LC-grown cells (p<0.01).
The C / N ratio showed no significant difference among different
temperatures in the HC treatment (p>0.05, Fig. 4b). In the LC treatment,
the C / N ratio was significantly higher at 24 ∘C than that at
15 and 20 ∘C (p<0.05). The C / N ratio in the LC treatment
was 9.5 % higher than that in the HC treatment at 24 ∘C (p<0.05), while the value showed no significant difference between the HC and LC
treatments at 15 and 20 ∘C (p>0.05).
Responses of photosynthetic carbon fixation to UV radiation
After 3 h of exposure under the solar simulator, significant interactive
effects between temperature and irradiance (p<0.01), temperature and
pCO2 (p<0.01), and irradiance and pCO2
(p=0.042) were observed on photosynthetic carbon fixation (Table 3). There were no
differences in photosynthetic carbon fixation rates between HC- and
LC-cultures at 15 ∘C under the PAR only treatment (p>0.05,
Fig. 5a), while the values were marginally (p=0.064, Fig. 5b) and
significantly (p=0.026, Fig. 5c) higher in HC-grown cells compared with
LC-grown cells at 20 and 24 ∘C. At 15 ∘C, presence of UVA or
UVR (UVA + UVB) had no significant effect on the photosynthetic rate under
the LC conditions (p>0.05); however, it lowered the photosynthetic rate
under the HC conditions (p<0.01, Fig. 5d). At 20 ∘C, the values
were reduced by 33.4 % (p<0.05) and 19.9 % (p=0.05) in HC- and
LC-grown cells under the PA treatment compared with the PAR only treatment
(Fig. 5b, e). The PAB treatment did not further lower the photosynthetic
rates compared to the PA treatment in either the HC- or LC-cultures (p>0.05). At the highest temperature of 24 ∘C, the photosynthetic rate
was 22.6 % (p<0.01) and 34.8 % (p<0.01) lower under the PA
treatment compared to the PAR only treatment in HC- and LC-grown cells,
respectively (Fig. 5c, f). The values were further decreased by 35.7 %
(p<0.01) in HC-grown cells, but were not affected in LC-grown cells in the
PAB treatment (p>0.05).
Calcification rates under P, PA and PAB (a–c); inhibition
of calcification rates due to UVA, UVB and UVR (d–f); and
Cal / Pho ratios under P, PA and PAB (g–i) for E. huxleyi in HC- and LC-grown cells at 15, 20 and 24 ∘C. Negative
inhibition values indicate stimulation. Lines above the histogram bars
indicate significant differences between the HC and LC treatments, and the
different letters indicate significant differences among the radiation
treatments within the HC or LC-grown cells within each panel.
Calcification rates and Cal / Pho ratios in response to UV
exposures
Calcification rates were significantly lower in HC-grown cells compared with
LC-grown cells under the PAR only treatment at all temperature levels (p<0.01, Fig. 6a–c). The PA treatment significantly increased the
calcification rate in HC-grown cells relative to the PAR only treatment by
31.7 % (Fig. 6a, d), 18.9 % (Fig. 6b, e) and 30.3 % (Fig. 6c, f)
at 15, 20 and 24 ∘C, respectively (p<0.05). However, there were no
significant differences in calcification rates between PA and PAR treatments
in LC-grown cells (p>0.05). Under the PAB treatment, the presence of UVB
led to a reduced calcification rate compared with the PA treatment at
15 ∘C (p<0.01). This inhibition was significantly higher in HC-cultures
compared to LC-cultures (Fig. 6a, d), but there were no significant
differences in the calcification rates between the PA and PAB treatments at 20 and
24 ∘C (p>0.05) in either HC- or LC-grown cells. There were
significant interactions between temperature and irradiance on the calcification
rate (p=0.018).
Mean values of the seawater carbonate system parameters under HC
(1000 µatm) and LC (400 µatm) at 15, 20 and
24 ∘C. The cell concentrations of all cultures were maintained below
5×104 cells mL-1 and pH variations were <0.04
units.
Treatment
pHNBS
DIC
pCO2
HCO3-
CO32-
Total alkalinity
(µmol kg-1)
(µatm)
(µmol kg-1)
(µmol kg-1)
(µmol kg-1)
15 ∘C
HC
7.80±0.02a
2147.2±105.7a
1000±40a
2037.5±98.6a
72.4±7a
2228.5±114.4a
LC
8.13±0.01b
1919.2±27.2b
400±40b
1768.1±23.6b
136.2±3.6b
2122.8±31.7a
20 ∘C
HC
7.82±0.01a
2153.2±57.3a
1000±40a
2031.5±52.8a
89.74±4.5a
2262.7±62.9a
LC
8.16±0.01b
1961.8±25.7b
400±40b
1777.8±21.8b
170.13±3.9b
2214.38±30.4a
25 ∘C
HC
7.84±0.01a
2057.2±28.1a
1000±40a
2174.8±26.2a
106.3±2.5a
2310.3±31.2a
LC
8.18±0.01b
1854.6±46.5b
400±40b
1999.8±38.4b
203.1±8.2b
2297.2±56.4a
The superscripts letters represent a significant difference between HC and
LC (p<0.05).
The optimal temperature for growth (Topt) and the maximum
growth rate (μmax) at Topt for E. huxleyi grown in
400 µatm (LC) and 1000 µatm (HC) CO2
concentrations. Topt and μmax as estimated from the fitted
curves in Fig. 1 by numerical optimization.
Topt (∘C)
μmax (μ)
HC
20.58
1.22
LC
22.15
1.31
Three-way ANOVA analyses of interactive effects among
pCO2 (CO2), temperature (T) and irradiance (I,
including P, PA and PAB) on photosynthetic carbon fixation rates,
calcification rates and Cal / Pho ratios, respectively. Also shown are
three-way ANOVA analyses of interactive effects among CO2
(CO2), temperature (T) and irradiance (I, including UVA, UVB and
UVR) on the inhibition (Inh) of photosynthesis (Pho), calcification (Cal) and the Cal / Pho
ratios, respectively.
T×I
T×CO2
I×CO2
T×I×CO2
p (df, F)
p (df, F)
p (df, F)
p (df, F)
Pho rate
<0.01**
<0.01**
0.042*
0.055
(4, 7.220)
(2, 11.505)
(2, 3.453)
(4, 2.560)
Cal rate
0.018*
0.541
0.465
0.483
(4, 3.432)
(2, 0.625)
(2, 0.783)
(4, 0.885)
Cal / Pho ratio
<0.01**
0.03*
0.632
0.002**
(4, 8.253)
(2, 3.874)
(2, 0.464)
(4, 5.155)
Inh of Pho rate
0.231
0.381
0.565
<0.01**
(4, 1.473)
(2, 0.991)
(2, 0.580)
(4, 8.546)
Inh of Cal rate
0.01**
0.24
<0.01**
<0.01**
(4, 3.928)
(2, 1.484)
(2, 8.881)
(4, 6.610)
Inh of Cal / Pho ratio
0.021*
0.108
0.127
<0.01**
(4, 3.331)
(2, 2.365)
(2, 2.186)
(4, 6.727)
* and ** represent significance levels at p<0.05 and
0.01, respectively.
The calcification to photosynthesis ratio (Cal / Pho ratio) values were
significantly higher under PA than in the PAR only treatment (p<0.05, Fig. 6g–i), regardless of the CO2 concentrations and
temperature levels. The Cal / Pho ratio was lower at 15 ∘C under
PAB compared with the PA treatment in both HC-grown (p<0.01) and LC-grown (p<0.05) cells,
while there were no significant differences between these
irradiance treatments at 20 and 24 ∘C (p>0.05). Except in the PA
treatment at 15 ∘C, the Cal / Pho ratio was significantly lower
in HC-grown cells compared with LC-grown cells under all of the other conditions,
with the greatest reduction of 44.3 % at 24 ∘C. There were
significant interactions among all three variables for the Cal / Pho
ratio (p<0.01).
Discussion
Our results demonstrated that both photosynthesis and calcification were
inhibited by UVB. In contrast, UVA was more inhibitory for photosynthesis
than UVB, while it had a positive effect on calcification. The degree to
which UVA and UVB affected the performance of photosynthesis and
calcification varied depending on CO2 concentrations and temperature
levels. Of the three temperature levels used, 15 ∘C was much lower
than the optimal growth temperature for both HC- and LC- grown cells. For LC
cultures, the growth rate was the same at 20 and 24 ∘C, and these
two temperatures were in the optimal range for cell growth. While
20 ∘C was very close to the optimal temperature for HC-grown cells,
the growth rate at 24 ∘C was significantly reduced, suggesting that the
cell growth at this temperature may already be thermally inhibited. The
different growth state among the three temperature levels, particularly that
between HC- and LC-grown cells at the highest temperature, potentially
affected the photosynthetic and calcification responses to UV radiation.
In this study, the inhibition of photosynthesis by UVA, UVB and their
combination appeared to increase with temperature. On the contrary, previous
studies conducted on other phytoplankton species such as diatoms have suggested
that increasing temperature could reduce UV-induced inhibition of
photosynthesis, as the activities of repair-associated enzymes are
temperature dependent (Li et al., 2012; Helbling et al., 2011). These
differing trends between the present work and previous studies may be attributed
to either changes in the thickness of the coccolith layer surrounding the
cells, or to the temperature range used. The coccoliths of E. huxleyi can play a protective role against UVR by either strongly
scattering light, or by physically shading intracellular organelles (Xu et
al., 2016; Voss et al., 1998). In our results, the cellular PIC at
20 ∘C was only half of that at 15 ∘C. As cellular PIC is
an indicator of the amount of coccoliths on the exterior of the cell, this
suggests that the cells grown at 20 ∘C had a substantially thinner
coccolith layer and consequently received much more UV radiation, leading to increased
photosynthetic damage compared with cells grown at 15 ∘C. At
24 ∘C, the thermal reaction curves suggested that this temperature
level was already close to the upper tolerance limit for growth in E. huxleyi PML B92/11, with HC-grown cells suffering more thermal stress. At
this temperature, although the thickness of the coccolith layer was equal to that
at 15 ∘C, biochemical aspects of UVR defense and/or repair
mechanisms may be under thermal stress (Sobrino and Neale, 2007).
At 15 and 20 ∘C the inhibition of photosynthesis was mainly caused
by UVA, and the values were significantly higher in HC-grown cells compared
with LC-grown cells, due to a thinner coccolith layer on cells in acidified
seawater (Gao et al., 2009). In contrast, at 24 ∘C the HC treatment
alleviated the UVA-induced inhibition compared with the LC treatment but also
greatly enhanced inhibition by UVB. The underlying mechanism may be
protein-mediated defense/repair processes. This is supported by the fact that
the C / N ratio was only increased by the LC treatment at 24 ∘C.
The C / N ratio can reflect the defense and repair ability of cells
against UVR (Sobrino et al., 2008; Litchman et al., 2002). Phytoplankton use
several mechanisms to repair UV-induced damage, many of which involve
nitrogen-requiring enzymes and/or protein cofactors (Litchman et al., 2002). Korbee
et al. (2010) reported that UVA could stimulate algae nitrogen metabolism (nitrate
transport and reductase activity). In contrast, UVB was found to damage cell
membranes and negatively affect nitrogen incorporation mechanisms, leading to
an increase in the C / N ratio (Sobrino et al., 2004). Such a
lack of nitrogen would subsequently inhibit essential protein turnover. In our study at
24 ∘C, UVA and HC might act synergistically to maintain a lower
C / N ratio and support the synthesis of UV-repair proteins, thereby
partially counteracting the UV-induced damage. As mentioned above, at
24 ∘C HC-grown cells were already thermally inhibited, which may add
the detrimental effect of UVB on nitrogen assimilation and lead to a much
higher inhibition of photosynthesis by UVB in high CO2, warmer
conditions.
When assessing the effect of UV radiation on calcification, we found that UVA
stimulated the calcification rate of E. huxleyi PML B92/11, while UVB
inhibited it. In earlier studies, Gao et al. (2009) reported that both UVA
and UVB negatively affected the calcification of E. huxleyi CS-369. One
possibility for this discrepancy between our studies can be attributed to
strain-specific responses. Conversely, the different irradiances used
by the two studies could also be involved, as the light intensity utilized by Gao et
al. (2009) was over twice as high as the one we used. Similarly to our study, Xu and
Gao (2015) also observed that moderate levels of UVR increased PIC production
rates. It has been demonstrated that E. huxleyi can use only
bicarbonate to support its calcification (Kottmeier et al., 2016; Paasche,
2002). Thus, the observed stimulation of calcification by UVA can perhaps be
attributed to UVA-enhanced bicarbonate utilization (Xu and Gao, 2010).
Given that the responses of coccolithophore strains to environmental change
can be different depending on the strain's temperature optimum (Sett et al.,
2014), the temperatures we chose in this study were below, close to or above
optimum for E. huxleyi growth based on its thermal tolerance curves.
The lower temperature of 15 ∘C that we used was around the mean
summer surface water temperature in the region where E. huxleyi PML
B92/11 was isolated (Fielding, 2013). A temperature of 20 ∘C, in
comparison, represents a future warmer condition, with 24 ∘C likely being
similar to the upper limit of temperatures that will be experienced by this
strain due to temperature fluctuations in the future. In the present study,
we found that UV radiation could interact with both temperature and
CO2 concentration to alter their effects on photosynthesis and
calcification, thus changing Cal / Pho ratios. The interactive effects of
elevated CO2 and UV radiation on non-calcifying marine organism have
been extensively reported (Li et al., 2012; Gao et al., 2012). With regard to
the calcifying coccolithophore E. huxleyi, OA
generally reduces their calcification (thinner coccolith layer) as well as
the Cal / Pho ratio, based on a number of indoor laboratory experiments
with UV-free light sources (Tong et al., 2018). In the present study, with
increasing temperature, we found that there was no significant difference in
the Cal / Pho ratios between high and low CO2-grown cells under UV
radiation at 24 ∘C. The light intensity used was equivalent to the
mean light level in the upper mixed layer (UML) based on time series station
(19∘ N, 118.5∘ E) measurements in the South China Sea. Our
results imply that E. huxleyi exposed to moderate levels of solar
radiation can sustain their cell density with a constant Cal / Pho ratio
under progressive warming and acidification. However, considering the slow
mixing of the upper layer during the daytime, cells dwelling in a shallower
UML are likely to be exposed to higher doses of solar irradiances. Under such
circumstances, UV radiation is most likely to reduce Cal / Pho ratios in
E. huxleyi, and ocean acidification will exacerbate the effect of UV
radiation (Gao et al., 2009). As a result, the net effects of temperature,
CO2 concentration and UV radiation will largely depend on the levels
of solar radiation to which the cells are exposed.
In previous studies, most indoor laboratory experiments neglected the effects
of UV radiation due to the common use of UV-free light sources or UV-opaque
vessels. Our results demonstrated that UV radiation could greatly influence
the combined effects of future CO2 enrichment and sea surface warming
on the physiological performance of E. huxleyi. Thus, the impacts UV
radiation should be considered in order to build more realistic predictions
of future biological and biogeochemical processes in a high-CO2
ocean.