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Abstract

Ocean acidification in response to rising atmospheric CO2 partial pressures is widely expected to reduce calcification by marine organisms. From the mid-Mesozoic, coccolithophores have been major calcium carbonate producers in the world's oceans, today accounting for about a third of the total marine CaCO3 production. Here, we present laboratory evidence that calcification and net primary production in the coccolithophore species Emiliania huxleyi are significantly increased by high CO2 partial pressures. Field evidence from the deep ocean is consistent with these laboratory conclusions, indicating that over the past 220 years there has been a 40% increase in average coccolith mass. Our findings show that coccolithophores are already responding and will probably continue to respond to rising atmospheric CO2 partial pressures, which has important implications for biogeochemical modeling of future oceans and climate.
DOI: 10.1126/science.1154122
, 336 (2008); 320Science
et al.M. Debora Iglesias-Rodriguez,
World2Phytoplankton Calcification in a High-CO
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Phytoplankton Calcification in a
High-CO
2
World
M. Debora Iglesias-Rodriguez,
1
* Paul R. Halloran,
2
* Rosalind E. M. Rickaby,
2
Ian R. Hall,
3
Elena Colmenero-Hidalgo,
3
John R. Gittins,
1
Darryl R. H. Green,
1
Toby Tyrrell,
1
Samantha J. Gibbs,
1
Peter von Dassow,
4
Eric Rehm,
5
E. Virginia Armbrust,
5
Karin P. Boessenkool
3
Ocean acidification in response to rising atmospheric CO
2
partial pressures is widely expected
to reduce calcification by marine organisms. From the mid-Mesozoic, coccolithophores have
been major calcium carbonate producers in the worlds oceans, today accounting for about a
third of the total marine CaCO
3
production. Here, we present laboratory evidence that
calcification and net primary production in the coccolithophore species Emiliania huxleyi are
significantly increased by high CO
2
partial pressures. Field evidence from the deep ocean is
consistent with these laboratory conclusions, indicating that over the past 220 years there has been
a 40% increase in average coccolith mass. Our findings show that coccolithophores are already
responding and will probably continue to respond to rising atmospheric CO
2
partial pressures,
which has important implications for biogeochemical modeling of future oceans and climate.
T
he climatological and ecological impacts
of elevated atmospheric CO
2
partial pres-
sures (P
CO
2
) are two of the most pressing
environmental concerns of the present. One con-
sequence of increasing P
CO
2
in seawater is the
formation of carbonic acid (H
2
CO
3
), which causes
acidification. Carbonic acid combines with car-
bonate ions (CO
3
2
)andwatermoleculestoform
bicarbonate ions (HCO
3
), reducing [CO
3
2
]and
the oceans saturation state with respect to calcite
(W-cal), the form of calcium carbonate (CaCO
3
)
produced by coccolithophores. Elevated P
CO
2
also causes an increase in [HCO
3
], the source
of carbon for calcification in coccolithophores
(Ca
2+
+2HCO
3
CaCO
3
+CO
2
+H
2
O) (1).
Thus,calcificationisprobablyaffectedbyin-
creasing P
CO
2
. The precipitation from seawater of
CaCO
3
, a basic substance, lowers pH. For this
reason, and because a greater fraction of dissolved
inorganic carbon {DIC, the sum of HCO
3
,CO
3
2
,
and aqueous CO
2
[CO
2
(aq)]} is present as CO
2
(aq)
at low pH, the formation of CaCO
3
in seawater
stimulates an increase in the concentration of
CO
2
(aq) and promotes its outgassing. Conse-
quently, a decrease in marine calcification with-
out a concomitant decrease in organic carbon
export would lead to an increased drawdown of
atmospheric CO
2
.
Recent evidence suggests that the increased
absorption of CO
2
by the oceans, as a result of an-
thropogenic CO
2
release, will result in decreased
calcification by corals (2), foraminifera (3), and
coccolithophores (46). However, it has recently
been shown that different coccolithophore spe-
cies exhibit different calcification responses. Un-
der increased P
CO
2
, a decrease in calcification has
been observed for Emiliania huxleyi and Gephyr o-
capsa oceanica (46); a negligible calcification
change with rising P
CO
2
for Coccolithus pelagicus
(7); and an increase followed by a decrease in cal-
cification with rising P
CO
2
, with respect to present-
day P
CO
2
,forCalcidiscus leptoporus (7). Most of
these experiments used semicontinuous cultures, in
which the carbonate system was modified by the
addition of acid and/or base to control pH (4, 5, 7).
Seawater pH controls the relative proportion of
the carbonate species while the concentration of
DIC remains constant. A more realistic representa-
tion of the ocean response to anthropogenic change
is the bubbling of CO
2
-enriched air th rough the
seawater , both elevating [DIC] and decreasing
pH. Recent studies with various organisms show
calcification to be largely controlled by W-cal, rath-
er than pH alone (7, 8), and W-cal is controlled by
both [ DIC] and pH. Between the years 1800 and
2100, seawater pH is likely to fall from 8.2 to 7.8
(9). Achieving the required pH by CO
2
bubbling
induces a greater percentage increase in [HCO
3
]
than when the same pH reduction is achieved
through acid addition (which does not affect [DIC]).
Therefore, to investigate calcification under future
CO
2
scenarios, it is important to correctly simulate
[HCO
3
].
We designed experiments that accurately rep-
resent projections of the future carbonate system,
and assessed the natural response of coccolitho-
phores in the sedimentary record to infer these
relationships over the past two centuries. Labora-
tory experiments tested the effect of increasing
P
CO
2
on calcification and other physiological pa-
rameters in the globally important coccolithophore
species E. huxleyi. W e then considered the lab-
oratory results in the context of a field study , using
sediment material from the box core RAPID 21-
12-B (10) to examine assemblagewide changes in
coccolith mass over the past ~220 years in response
to anthropogenic CO
2
release.
Culture experiments. We conducted batch
incubations with exponentially growing cells of
the coccolithophore species E. huxleyi (11). Com-
mercially manufactured air containing different
P
CO
2
was bubbled through the culture medium
to adjust the P
CO
2
of cultures from preindustrial
levels [280 parts per million by volume (ppmv)
of CO
2
] up to the level predicted by one scenario
for the end of the 21st century (750 ppmv of CO
2
)
(12). Our results suggest a doubling of particu-
late inorganic carbon (PIC) and particulate or-
ganic carbon (POC) production at 750 ppmv of
CO
2
. Between 280 and 490 ppmv , carbon metab-
olism remained broadly similar . In contrast, be-
tween 490 and 750 ppmv, both cellular PIC and
POC and their production rates increased signif-
icantly (Fig. 1 and table S1). Growth rates were
substantially lower at 750 ppmv of CO
2
as com-
pared with 280, 300, and 490 ppmv of CO
2
(Fig.
1 and table S1). In parallel to the increases in
POC and PIC production, analyses of particle
counts and volumes (Coulter counter and flow cy-
tometry analysis) were conducted in a subset of
experiments. These analyses demonstrated that the
volumes of both coccospheres (protoplast and cal-
cium carbonate plates or coccoliths) and coccoliths
increased with rising P
CO
2
, following a similar trend
in PIC and POC (Fig. 2 and Table 1). The range of
coccolith volumes is comparable to that reported in
response to changing nutrient availability and salin-
ity (13). Flow cytometry data indicated that the
PIC increase in the medium under high P
CO
2
was
due to both an increase in the volume of calcite
within the coccospheres and an increase in the
production of detached coccoliths (T able 1). Scann-
ing electron micrographs of cells did not reveal
apparent malformation or dissolution of coccoliths
under any of the experimental P
CO
2
conditions
(Fig. 2). Physiological changes related to increased
PIC and POC production were not accompanied
by alterations in the photochemical efficiency of
photosystem II [the ratio of the variable-to-
maximum fluorescence (Fv:Fm) ~ 0.48] (14), as-
sessed using fast repetition rate fluorometry (FRRF)
(14), indicating that cells remained photo-
synthetically healthy in all experiments (Fig. 1).
A key factor determining whether coccolitho-
phore production represents a net source or sink of
CO
2
to the atmosphere is whether the calcification-
to-photosynthesis ratio is greater or less than 1.5
(15, 16). The coincident increase in both PIC and
POC production per cell in all the P
CO
2
treatments
resulted in a stable PIC:POC ratio of less than 1,
although interactions with other climate-driven
parameters may affect the observed trends. Our
RESEARCH ARTICLES
1
National Oceanography Centre, Southampton, University
of Southampton Waterfront Campus, European Way,
Southampton SO14 3ZH, UK.
2
Department of Earth
Sciences, University of Oxford, Parks Road, Oxford OX1
3PR, UK.
3
School of Earth, Ocean and Planetary Sciences,
Cardiff University, Main Building, Park Place, Cardiff CF10
3YE, UK.
4
Station Biologique de Roscoff, Place George
Teissier, BP 74, 29682 Roscoff Cedex, France.
5
School of
Oceanography, Box 357940, University of Washington,
Seattle, WA 98195, USA.
*These authors contributed equally to this work.
Present address: Departamento de Geología, Facultad de
Ciencias, Universidad de Salamanca, 37008 Salamanca, Spain.
18 APRIL 2008 VOL 320 SCIENCE www.sciencemag.org336
on April 21, 2008 www.sciencemag.orgDownloaded from
results suggest that levels of PCO
2
and W-cal cor-
responding to projections for the end of this cen-
tury are unlikely to affect the metabolic balance
between organic carbon fixation and calcite pre-
cipitation in E. huxleyi.
We measured the ratios of POC to particulate
organi c nitrogen (C:N) to assess whether the ele-
mental composition of the organic material was
additionally affected by changing P
CO
2
. Variations
in the elemental stoichiometry of phytoplankton
are known to have an effec t on trophic interactions,
because the dietary value of prey items for marine
zooplankton varies with the C:N ratio (17). Pre-
vious studies have reported changes in the elemen-
tal composition of diatoms in response to variations
in P
CO
2
(18). The C:N ratios in E. huxleyi increased
from 6.8 to 8.3 with rising P
CO
2
between 280 and
750 ppmv of CO
2
(Fig. 1). These results indicate
that the P
CO
2
could affect the grazing-selection
pressure on phytoplankton, representing different
food qualities. Grazing selection has many bio-
geochemical consequences and in particular impli-
cations for the export flux of carbon (17).
Our data show that W-cal ranged from 5.3 at
280 ppmv of CO
2
to 2.6 at 750 ppmv of CO
2
,cor-
responding to an average total alkalinity of 2292
meq liter
1
(Table 2). W-cal values were within the
range of those for most of the upper-ocean regions,
and well above 1, the threshold value below which
dissolution would occur . In this pH range, less
than 10% of the DIC in the medium was taken up
by the proliferating cells (T able 2). Comparing
these values with those in the corresponding blanks
(without E. huxleyi c e ll s ) shows that cell physiol-
ogy caused a shift in pH of less than 0.04 units in
all experiments (Table 2). The pH values of the
cultures incubated at 280 and 750 ppmv of CO
2
ranged between 8.1 and 7.7 (corresponding to 9.5
mMCO
2
and 25.1 mMCO
2
, respectively). These
changes did not affect the photosynthetic health of
cells (Fig. 1), which implies our pH conditions
were within the tolerance levels of E. huxleyi.A
Fig. 1. Cellular PIC (A), POC (B), PIC production
rates (C), POC production rates (D), C:N ratios (E),
PIC:POC ratios (F), growth rates (G), and Fv:Fm (H)
for E. huxleyi cultures under different P
CO
2
.Each
color represents one independent experiment.
Significant increases with rising P
CO
2
were observed
for PIC (F
4,16
= 24.14, P <0.001),POC(F
4,9
=
10.23, P = 0.002), PIC production (F
4,16
=5.94,P =
0.004), POC production (F
4,9
=4.52,P = 0.028),
and growth rate (F
4,16
=3.92,P = 0.021) (table S1).
Differences between the treatments of 600 and 750
ppmv of CO
2
were significant for PIC (P =0.002)but
nonsignificant (P > 0.05) for all other parameters.
Cellular PIC and POC were comparable at 280, 300,
and 490 ppmv of CO
2
. Above 490 ppmv of CO
2
,
cellular PIC and POC increased significantly, by 80
and 90% respectively at 600 ppmv of CO
2
,andbya
further 48 and 45% respectively at 750 ppmv of
CO
2
. Variation in PIC and POC production rates
between 280 and 490 ppmv was not significant
(table S1). Between 490 and 600 ppmv of CO
2
,PIC
and POC production rates increased by approxi-
mately 44 and 81%, respectively, and these were
approximately 30 and 18% higher at 750 than at
600 ppmv of CO
2
. Growth rates were significantly
lower at 750 ppmv of CO
2
as compared with 280,
300, and 490 ppmv of CO
2
. Differences in PIC:POC
under th e different P
CO
2
treatments were nonsig-
nificant (F
4,9
=1.22,P = 0.368) (table S1). The C:N
values increased from 6.8 at 280 ppmv of CO
2
to
8.3 at 750 ppmv of CO
2
.Fv:Fmvalueswerecom-
parable in all P
CO
2
treatments. The shaded area
represents putative P
CO
2
during the PETM [lower-
end estimates of P
CO
2
were based on stomatal index
and boron isotopes, data compiled in (38)].
0.8
0.6
0.0
1.2
100
2000 300 400 500 600 700 800
0.0
0.4
0.6
0.8
1.0
200 300 400 500 600 700 800
100
100
2000 300 400 500 600 700 800
0.0
0.8
1.0
1.2
A
0.5
B
CD
1
2
3
4
5
6
7
8
E
G
H
100
2000 300 400 500 600 700 800
0.0
0.5
1.0
1.5
2.0
PIC (pmol CaCO
3
cell
-1
)
POC (pmol C cell
-1
)
100
2000 300 400 500 600 700 800
0.0
1.0
1.5
2.0
0.6
0.4
0.2
PIC prod (pmol CaCO
3
cell
-1
d
-1
)
0
0
C:N ratio
0.2
Growth rate (d
-1
)
ρCO
2
Fv:Fm
100
2000 300 400 500 600 700 800
0.2
0.4
1.0
100
2000 300 400 500 600 700 800
0.0
0.2
0.6
0.8
1.0
F
0.4
PIC:POC ratio
POC prod (pmol C cell
-1
d
-1
)
100
2000 300 400 500 600 700 800
0.0
0.2
0.4
0.6
ρCO
2
Fig. 2. Coccolith volume and CaCO
3
per cell. Increasing coccolith volume is closely coupled with
increasing CaCO
3
per cell, indicating down-core measurement of coccolith mass to be representative of
CaCO
3
production. Scanning electron microscope (SEM) images show typical coccoliths from each
culture with P
CO
2
values from 280 to 750 ppmv of CO
2
, of where the measured volume was converted
to length using the formula for a heavily calcified coccolith (27).
www.sciencemag.org SCIENCE VOL 320 18 APRIL 2008
337
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similar conclusion was reached in (19), where pH
values within the range of those measured here
did not suppress calcification. Our results are un-
likely to be due to the physiological traits of a
particular strain of E. huxleyi, because we ob-
served the same effects on calcification and or-
ganic carbon production in another calcifying
strain of E. huxleyi (61/12/4, Marine Biological
Association, Plymouth, UK).
Down-core observations. In light of our lab-
oratory results, which show a correlated increase
in PIC and coccolith size with elevated P
CO
2
,we
investigated the response of a natural coccolitho-
phore assemblage at high latitude to anthropogenic
ocean acidification since the Industrial Revolution.
We developed a method that can estimate the av-
erage mass of calcite per coccolith across multiple
coccolithophore taxa (11). This technique was ap-
plied to material from the box core RAPID 21-12-B
(57°27.09N, 27°54.53 W), situated at 2630 m
water depth in the subpolar North Atlantic. Core
RAPID 21-12-B contains unprecedented open-
ocean sedimentation rates of 2.3 mm year
1
spanning the time interval from 1780 to 2004 C.E.
(10), which allows a detailed view of coccolith
formation over the Anthropocene period, the
period of anthropogenic CO
2
release.
Sediment was filtered at 10 mm to obtain the
coccolith fraction, excluding larger carbonate
grains (11) (fig. S1). The mass of calcite in two
subsamples at each depth was measured in trip-
licate, and the number of CaCO
3
particles between
0.63 and 10 mm [reasonably assumed to be cocco-
liths (20, 21)] was counted nine times with an
electrical resistance pulse detector (Coulter counter).
Measurements were made before and after the
addition of acid to account for the non-CaCO
3
component of the sediment. An upper detection
limit of 10 mm was chosen to focus observa tions
on particles with cohesive behavior and to avoid
sampling the drift component of the sediment (22).
This method excludes coccoliths with a diameter
>10 mm. Only coccoliths of C. pelagicus braarudii
were consistently >10 mm and were correspond-
ingly excluded from the species counts. This ap-
proach measures the average mass of calcite per
coccolith, which integrates any change in CaCO
3
mass due to variations in the assemblage and to
intraspecies shifts in coccolith mass. T o examine
whether changes in species composition could
account for the observed trend, coccolith assem-
blages were counted under a light microscope, fol-
lowing standard techniques for preparation by
settling (23). No significant trend in species com-
position (Fig. 3) nor estimated species mass
contribution (fig. S2) was observed. Dividing au-
tomated particle counts by sample weights before
and after the removal of CaCO
3
by dissolution,
and subtracting postdissolution measurements
from predissolution measurements, not only
rapidly provided average mass data on a large
number of coccoliths (average sample counts
were ~80,000 CaCO
3
particles), but was also
sensitive to volume changes in the coccolith in any
dimension.
The average mass of CaCO
3
per coccolith
increased from 1.08 × 10
11
to 1.55 × 10
11
g
between 1780 and the modern day (Fig. 4), with
an accelerated increase over recent decades (fig.
S3). Evidence is building that coccoliths are more
resistant to dissolution than are planktonic fo-
raminifera (24) and that they remain pristine
when exposed to fluids in the pH range of 6 to 8
(25). In agreement with these observations, the
absence of any down-core trend in coccolith
species abundance in RAPID 21-12-B, despite
the presence of taxa exhibiting a range of suscep-
Table 1. Coccosphere and coccolith volumes of E. huxleyi cells under different PCO
2
measured using
a Coulter counter and flow cytometer. t tests of pairwise comparisons of the mean coccosphere and
coccolith volumes measured by Coulter counter gave P values below 0.01 for all the pairwise
comparisons. Side scatter (here in relative units, normalized to the side scatter of 3-mm internal
bead standards) correlates strongly with the cellular calcification of E. huxleyi (39), whereas forward
scatter correlates with coccosphere size. Comparison of forward-scatter volume before and after
acidification indicates that the differences in volume among the different P
CO
2
were due both to the
amount of calcite and to the size of the organic protoplast. The difference between Coulter counter
versus flow cytometer volume measurements may be an effect of the different ways that the volume
is calculated by these two instruments (electronically versus optically). nd, not determined.
Coulter counter Flow cytometer
P
CO
2
Average
coccosphere
Coulter
volume
(mm
3
)
Average
coccolith
volume
(mm
3
)
Average
coccosphere
side scatter
(relative to 3-
mm beads)
(relative
units)
Coccosphere
forward-scatter
volume
before/after
acidification
(mm
3
)
Average
number of
detached
coccoliths
per
coccosphere
280.00 55.44 1.09 3.86 115/66.1 13.2
303.79 45.95 0.84 3.84 111/57.4 10.3
489.18 65.13 1.11 3.89 123/63.6 24.2
595.09 55.23 1.84 nd nd nd
750.25 69.33 1.86 4.05 155/77.1 80.3
Table 2. Carbonate chemistry in E. huxleyi cultures corresponding to different CO
2
scenarios from
preindustrial time to projections for the end of this century (11). For each parameter, the numbers
in the first row represent average values measured in the exponential growth phase, the numbers in
the second row represent the blank values at the beginning of the experiment, and the values in the
third row correspond to 1 SD of three samples.
Parameter Preindustrial Circa 1930 2035 2060 2100
P
CO
2
(ppmv) 280.0 303.8 489.2 595.1 750.2
268.2 326.3 524.8 726.2 844.1
0.3 0.2 3.5 9.2 3.0
[CO
2
](mmol liter
1
) 9.5 10.2 16.4 19.9 25.1
9.0 10.9 17.6 24.3 28.2
0.0 0.0 0.1 0.3 0.1
[CO
3
](mmol liter
1
) 222.7 215.0 157.3 112.1 108.5
244.0 216.4 157.7 123.3 110.0
0.3 0.0 0.8 1.4 0.4
[DIC] (mmol liter
1
) 1906.9 1923.5 2016.7 1848.1 2028.9
1952.6 1993.2 2086.4 2136.1 2162.6
0.7 0.6 1.0 1.1 0.2
[HCO
3
](mmol liter
1
) 1674.7 1698.2 1843.0 1716.0 1895.3
1699.6 1765.8 1911.2 1988.4 2024.4
0.3 0.6 1.7 2.2 0.4
W-calc 5.34 5.16 3.77 2.69 2.60
5.85 5.19 3.78 2.96 2.64
0.00 0.00 0.02 0.03 0.01
pH 8.15 8.13 7.96 7.85 7.79
8.19 8.12 7.95 7.82 7.77
0.00 0.00 0.00 0.01 0.00
Alkalinity (meq liter
1
) 2220.3 2224.9 2227.6 1995.9 2161.7
2294.0 2292.8 2294.6 2288.3 2291.6
1.2 0.6 0.3 1.3 0.4
18 APRIL 2008 VOL 320 SCIENCE www.sciencemag.org338
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tibilities to dissolution, indicates that our observed
increase in coccolith mass cannot be accounted
for by changing species compositions or dissolu-
tion effects (26).
The increase of ~ 4.5 pg in the average mass
of CaCO
3
per coccolith since ~1960, as indicated
by the smoothed least-squares curve in Fig. 4,
coincides with rising atmospheric P
CO
2
and is
consistent in direction and relative magnitude
with changes demonstrated here using laboratory
experiments with E. huxleyi under future CO
2
sce-
narios. On average, 75% by mass of the <10-mm
calcite (calculated by multiplying coccolith counts
by typical coccolith volumes) at site RAPID 21-
12-B constitutes coccoliths of only two taxa, C.
pelagicus pelagicus and Calcidiscus leptoporus,
and just 3.2% comes from E. huxleyi (fig. S2).
Ty pical coccoliths of the massive C. pelagicus
pelagicus and Calcidiscus leptoporus species are
approximately 15 and 7 times the average pre-1960
coccolith mass, respectively (27), and C. pelagicus
pelagicus alone would require a < 5% increase in
coccolith mass (equivalent to a ~ 0.25-mmdiam-
eter increase) to account for the entire observed
coccolith mass change, which is well within present-
day variability (27). Therefore, because changes
in the average coccolith mass can be dominated
by only a small number of heavily calcifying spe-
cies, it is quite possible that the global calcification
response may vary greatly with coccolithophore
species assemblage in alternative oceanic regimes.
However , the dominance of C. pelagicus pelagi-
cus over the sedimentary calcite mass observed in
this core is typical within the North Atlantic (2729),
and therefore our findings probably represent a
regional response, the response of a basin highly
sensitive to anthropogenic CO
2
production (9). If
species other than E. huxleyi also exhibit a con-
comitant increase in PIC and POC production
with rising CO
2
as demonstrated here for E. huxleyi,
there would be no net change in this ratio with
time, but we cannot quantify this ratio without a
record of total organic carbon production. Never-
theless, a potential consequence of increasing cal-
cification is a greater removal of POC from the
surface waters because of increased ballast effects
(30), although it is inconclusive whether or to
what degree increased CaCO
3
ballast would favor
arelativeincreaseinPOCexport(31).
Discussion. Delving into the geological re-
cord potentially provides additional insight into
coccolithophore response to elevated P
CO
2
.Pres-
ervation of calcareous nannofossils relies on a
buffering of the W-cal by vertical migration of the
calcite compensation depth (CCD), the depth at
which the rate of calcite input from surface wa-
ters equals the rate of dissolution. On time scales
of >10,000 years, the CCD buffer keeps W-cal
relatively constant (32); however, on shorter time
scales there have been intervals in the geological
past where the CCD has temporally shoaled, sug-
gesting ocean acidification and transient decreases
in carbonate saturation. The most widely studied
of these intervals is the Paleocene Eocene Thermal
Maximum (PETM, ~55 million years ago) (33).
Calcareous nannofossil records suggest no obvious
reduction in their abundance, shifts in distribution,
or evolu tionary bias attributable to ocean acidifi-
cation during the PETM (34). The pH and P
CO
2
reached in our culture experiments are within esti-
mates of those indicated for the PETM (Fig. 1),
and our laborato ry and field results are again con-
sistent with the lack of evidence for a change in satu-
ration state being detrimental to coccolithophores.
Our single-species culture experiments and
high-latitude assemblage records suggest that in a
scenario where the P
CO
2
in the worlds oceans
increases to 750 ppmv, coccolithophores will
double their rate of calcification and photosynthesis
(if ecosystem processes allow the survival of
similar numbers of larger coccolithophore cells in
the future). Given that coccolithophores are a
major contributor [about 50% (35)] to the open-
ocean carbonate pump, but a much smaller con-
tributor [about 10% (36)] to the soft-tissue pump,
we expect a disproportionate impact on overall
community rates of calcification. Our exper-
iments were conducted on E. huxleyi,whichforms
blooms at high latitudes that provide a snapshot of
the response of E. huxleyi to P
CO
2
under nutrient-
replete conditions. Previous work using chemostat
cultures under nutrient-limiting conditions (37)
showed that increasing P
CO
2
resulted in a decrease
Fig. 3. Relative percentage abundance of coccoliths of each species in RAPID 21-12-B counted under a
light microscope. No long-term trend in species composition was observed, indicating little or no
species response to anthropogenic forcing. Stasis in the species composition, as would be expected
considering the small temperature variation over this interval, implies that the core material is
unaffected by dissolution (26), which was confirmed by SEM examination. The observed species
assemblage is consistent with those published for other central subpolar Atlantic sites (27, 29).
Fig. 4. Average mass of
CaCO
3
per coccolith in
core RAPID 21-12-B and
atmospheric CO
2
.Theav-
erage mass of CaCO
3
per
coccolithincoreRAPID
21-12-B (open circles) in-
creased from 1.08 × 10
11
to 1.55 × 10
11
gbetween
1780 and the modern day,
with an accelerated in-
crease over recent decades.
Theincreaseinaveragecoc-
colith mass correlates with
rising atmospheric P
CO
2
,as
recorded in the Siple ice
core (gray circles) (26)and
instrumentally at Mauna
Loa (black circles) (38),
every 10th and 5th data
point shown, respectively.
Error bars represent 1 SD
as calculated from repli-
cate analyses. Samples with a standard deviation greater than 0.05 were discarded. The smoothed curve for
the average coccolith mass was calculated using a 20% locally weighted least-squares error method.
www.sciencemag.org SCIENCE VOL 320 18 APRIL 2008 339
RESEARCH ARTICLES
on April 21, 2008 www.sciencemag.orgDownloaded from
in net calcification rate and gross community
production but had no noticeable effect on the
ratio of calcification to photosynthesis. Other spe-
cies need to be investigated in light of the var-
iability encountered in response to changing P
CO
2
between coccolithophore species that are repre-
sentative of low and mid-latitudes (25).
Future research is needed to fully constrain
productivity changes over the Anthropocene pe-
riod, extend our understanding of calcification
changes at different latitudes and in different
ocean basins, and quantify how changing ballast
will affect export production. The widely held
assumption that all coccolithophores will decrease
their calcification under elevated P
CO
2
needs
reappraisal in the light of our laboratory and field
observations that demonstrate enhanced PIC pro-
duction and cell size under high P
CO
2
conditions
and the resilience of calcifying phytoplankton in
the geological record (34). Our analyses are high-
ly relevant to ocean biogeochemical modeling
studies and underline the physiological and
ecological versatility of coccolithophores and their
evolutionary adaptation through changes in ocean
carbonate chemistry associated with past and
projected P
CO
2
levels.
References and Notes
1. E. Paasche, Phycolog ia 49, 503 (2002).
2. J. A. Kleypas et al., Science 284, 118 (1999).
3. J. Bijma, H. J. Spero, D. W. Lea, B. E. Bemis, in Use of
Proxies in Paleoceanography: Examples from the South
Atlantic, G. Fischer, G. Wefer, Eds. (Springer, Berlin,
1999), pp. 489512.
4. U. Riebesell et al., Nature 407, 364 (2000).
5. I. Zondervan, R. E. Zeebe, B. Rost, U. Riebesell, Global
Biogeochem. Cycles 15, 507 (2001).
6. B. Delille et al., Global Biogeochem. Cycles 19, GB2023,
10.1029/2004GB002318 (2005).
7. G. Langer et al., Geochem. Geophy s. Geosyst. 7, Q09006
(2006).
8. S. Trimborn, G. Langer, B. Rost, Limnol . Oceanogr. 52,
2285 (2007).
9. R. A. Feely et al., Science 305, 362 (2004).
10. K. P. Boessenkool, I. R. Hall, H. Elderfield, I. Yashayaev,
Geophys. Res. Lett. 34, 10.1029/2007GL030285 (2007).
11. Materials and methods are available as supporting
material on Science Online.
12. K. Caldeira, M. E. Wickett, Nature 425, 365 (2003).
13. J. Bollmann, J. O. Herrle, Earth Planet. Sci. Lett. 255,
273 (2007).
14. Z. S. Kolber, O. Prasil, P. G. Falkowski, Biochim. Biophys.
Acta 1367, 88 (1998).
15. This balance point [the calcification-to-photosynthesis
ratio at which a bloom has zero net impact on
atmospheric CO
2
(C:P)] was calculated as having a
value of about 1.5 at [DIC] = 2050 mmol kg
1
, [Alk] =
2300 meq kg
1
, temperature = 15°C, and salinity = 35.
The value of the balance point C:P ratio exhibits some
variability with in situ conditions. For instance, it varies in
the range 1.0 to 1.8 as in situ conditions vary in the
ranges [DIC] = 2000 to 2300 mmol kg
1
, [Alk] = 2200 to
2400 meq kg
1
, temperature = 10 to 30°C and salinity =
33 to 37. Its value will decrease by about 20% as P
CO
2
increases from 280 ppmv to 700 ppmv (other conditions
remaining constant) (16).
16. M. Frankignoulle, C. Canon, J.-P. Gattuso, Limnol.
Oceanogr. 39, 456 (1994).
17. T. R. Anderson, P. Pondaven, Deep-Sea Res. I 50, 573 (2003).
18. S. Burkhardt, I. Zondevan, U. Riebesell, Limnol.
Oceanogr. 44, 683 (1999).
19. N. A. Nimer, M. J. Merrett, New Phytol. 123, 673 (1993).
20. H. Z. Wang, I. N. McCave, J. Geol. Soc. London 147, 373
(1990).
21. M. Frenz, K. H. Baumann, B. Boeckel, R. Hoppner,
R. Henrich, J. Sediment. Res. 75, 464 (2005).
22. I. N. McCave, I. R. Hall, Geochem. Geophys. Geosyst. 7,
Q10N05 (2006).
23. J. A. Flores, F. J. Sierro, Micropaleontology 43, 321 (1997).
24. M. Frenz, R. Henrich, Sedimentology 54, 391 (2007).
25. L. Beaufort, I. Probert, N. Buchet, Geochem. Geophys.
Geosyst. 8, Q09011, 10.1029/2006GC00149.
26. M. E. Hill, Micropaleontology 21, 227 (1975).
27. J. R. Young, P. Ziveri, Deep-Sea Res. II 47, 1679 (2000).
28. P. Ziveri, K. H. Baumann, B. Bockel, J. Bollmann,
J. You ng, in Coccolithophores: From Molecular Processes
to Global Impact, H. Thierstein, J. Young, Eds. (Springer,
Berlin, 2004), pp. 403428.
29. A. McIntyre, A. W. H. Bé, Deep-Sea Res. 14, 561 (1967).
30. D. Archer, E. Maier-Reimer, Nature 367, 260 (1994).
31. S. Barker, J. A. Higgins, H. Elderfield, Philos. Trans. R.
Soc. London Ser. A 361, 1977 (2003).
32. T. Tyrrell, R. E. Zeebe, Geochim. Cosmochim. Acta 68,
3521, 10.1016/j.gca.2004.02.018 (2004).
33. J. C. Zachos et al., Science 308, 1611 (2005).
34. S. J. Gibbs, P. R. Bown, J. A. Sessa, T. J. Bralower,
P. A. Wilson, Science 314, 1770 (2006).
35. K. H. Baumann, H. Andruleit, B. Bocke l, M. Geisen,
H. Kinkel, Palaontol. Z. 79, 93 (2005).
36. A. J. Poulton, T. R. Adey, W. M. Balch, P. M. Holligan,
Deep-Sea Res. II 54, 538 (2007).
37. A. Sciandra et al., Mar. Ecol. Prog. Ser. 261, 111 (2003).
38. D. L. Royer, R. A. Berner, I. P. Montañez, N. J. Tabor,
D. J. Beerling, GSA Today 14, 10.1130/1052-5173(2004)
0142.0.CO;2 (2004).
39. C. D. Keeling, T. P. Whorf, in Trends: A Compen dium
of Data on Global Change (Carbon Dioxide Information
Analysis Center, Oak Ridge National Laboratory, U.S.
Department of Energy, Oak Ridge, TN, 2005).
40. J. D. L. van Bleijswik, R. S. Kempers, M. J. Veldhuis,
J. Phycol. 30, 230 (1994).
41. The authors acknowledge M. Hill for manufacturing
the bubbling flasks, B. Alker for her assistance in PIC
preparation and analysis, D. Hydes for access to the
Versatile Instrument for the Determination of Titration
Alkalinity instrument, R. Head for POC analysis, and
R. Gibson for assistance with PIC and FRRF analysis.
We thank H. Medley for laboratory assistance and
J. Elliot for useful discussions. We are grateful to the
master, officers, crew, and scientific party of the RRS
Charles Darwin cruise CD159, in particular I. N. McCave
and H. Elderfield. We are grateful to O. M. Schofield,
P. A. Tyler, and T. Anderson for discussions on the
manuscript. We thank K. Davis for assistance with
graphic illustrations. This work was supported by
the Royal Society research grant no. 24437 (M.D.I.-R.)
and by the Betty and Gordon Moore Foundation Marine
Microbiology Investigator Award (flow cytometry analysis)
(E.V.A.). The field work was supported by the UK Natural
Environment Research Council RAPID Program. P.R.H.
acknowledges support from Natural Environment
Research Council (NERC) grant no. NER/S/S/2004/12772.
R.E.M.R. and I.R.H. gratefully acknowledge NERC
grant no. NER/T/S/2002/00980.
Supporting Online Material
www.sciencemag.org/cgi/content/full/320/5874/336/DC1
Materials and Methods
Figs. S1 to S3
Tables S1 and S2
References
13 December 2007; accepted 3 March 2008
10.1126/science.1154122
The Global Circulation of Seasonal
Influenza A (H3N2) Viruses
Colin A. Russell,
1
Terry C. Jones,
1,2,3
Ian G. Barr,
4
Nancy J. Cox,
5
Rebecca J. Garten,
5
Vicky Gregory,
6
Ian D. Gust,
4
Alan W. Hampson,
4
Alan J. Hay,
6
Aeron C. Hurt,
4
Jan C. de Jong,
2
Anne Kelso,
4
Alexander I. Klimov,
5
Tsutomu Kageyama,
7
Naomi Komadina,
4
Alan S. Lapedes,
8
Yi P. Lin,
6
Ana Mosterin,
1,3
Masatsugu Obuchi,
7
Takato Odagiri,
7
Albert D. M. E. Osterhaus,
2
Guus F. Rimmelzwaan,
2
Michael W. Shaw,
5
Eugene Skepner,
1
Klaus Stohr,
9
Masato Tashiro,
7
Ron A. M. Fouchier,
2
Derek J. Smith
1,2
*
Antigenic and genetic analysis of the hemagglutinin of ~13,000 human influenza A (H3N2)
viruses from six continents during 20022007 revealed that there was continuous circulation in
east and Southeast Asia (E-SE Asia) via a region-wide network of temporally overlapping epidemics
and that epidemics in the temperate regions were seeded from this network each year. Seed strains
generally first reached Oceania, North America, and Europe, and later South America. This evidence
suggests that once A (H3N2) viruses leave E-SE Asia, they are unlikely to contribute to long-term
viral evolution. If the trends observed during this period are an accurate representation of overall
patterns of spread, then the antigenic characteristics of A (H3N2) viruses outside E-SE Asia may
be forecast each year based on surveillance within E-SE Asia, with consequent improvements
to vaccine strain selection.
I
nfluenza A (H3N2) virus is currently the ma-
jor cause of human influenza morbidity and
mortality worldwide. On aver age, influenza
viruses infect 5 to 15% of the global population,
resulting in ~500,000 deaths annually (1). De-
spite substantial progress in many areas of influ-
enza research, questions such as when and to
what extent the virus will change antigenically,
and to what extent viruses spread globally , re-
main unanswered. A fundamental issue behind
these questions is whether epidemics are the con-
sequence of low-level persistence of viruses from
the previous epidemic or whether they are seeded
from epidemics in other regions and, if so, from
where (28).
Addressing these issues of local persistence
and global spread is vitally important for designing
optimal surveillance and control strategies. If epi-
demics were regularly seeded from an outside re-
gion and if the source region of seed strains could
be identified, it may be possible to forecast which
variants would appear in epidemics in seeded
18 APRIL 2008 VOL 320 SCIENCE www.sciencemag.org
340
RESEARCH ARTICLES
on April 21, 2008 www.sciencemag.orgDownloaded from
... The exact cause of the enhanced primary productivity during the PETM CIE is ambiguous at this point, however, based on the observations made in many recent studies, we opine that the enhanced atmospheric CO 2 concentrations probably triggered the algal growth during the PETM (Benedetti et al., 2021). Several laboratory experiments on plankton and algal growth under varying pCO 2 demonstrated that certain species of the plankton and algae show enhanced growth in high pCO 2 (Riebesell et al., 2007;Iglesias-Rodriguez et al., 2008;Packer, 2009;Singh and Singh, 2014) rather than the expected decalcification (Riebesell et al., 2000;Kurihara and Shirayama, 2004). Riebesell et al. (2007) reported that a marine plankton community, at high CO 2 partial pressure, consumed 39% more DIC while maintaining a constant nutrient uptake. ...
... Riebesell et al. (2007) reported that a marine plankton community, at high CO 2 partial pressure, consumed 39% more DIC while maintaining a constant nutrient uptake. Iglesias-Rodriguez et al. (2008) noticed increasing phytoplankton growth under high pCO 2 , similar to the amount that existed during the PETM. Singh and Singh (2014) also demonstrated the enhanced CO 2 consumption of certain macro-algae species in high pCO 2 conditions. ...
... To fill this lacuna, a few other studies proposed cyanobacterial nitrogen fixation (Knies et al., 2008), and phosphorous regeneration from sediments (Dickson et al., 2014) as possible sources of the nutrients for the algae growth in these shelves during the PETM. In line with these inferences, the higher pCO 2 during the PETM might have also played a vital role in the algal blooming (Iglesias-Rodriguez et al., 2008) even in the eutrophic shelves during the PETM (Schippers et al., 2004). As for oligotrophic shelves, like the present study area, where either a major river drainage system was low/ absent, or a high eustatic sea level curbed the terrestrial flux, the higher pCO 2 might have played a pivotal role in enhancing the primary productivity (Schippers et al., 2004). ...
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The coastal upwelling zones, occupying only ~0.5% of the global ocean, account for ~10% of the global primary productivity. The CO2 fixation by primary producers amplifies in the upwelling zones during global warming due to the higher nutrient supply. Based on the presumption that the nutrient-deficient coastal ocean is less productive, the state of the oligotrophic coastal ocean is often neglected in the productivity-climate change studies. The present study investigated the changes in the primary productivity, redox condition, and nutrient content, using algal abundance, total organic carbon, and various major, trace, and rare earth elements with yttrium (REY) proxies, of the oligotrophic equatorial eastern Tethyan coastal ocean across the Paleocene-Eocene Thermal Maximum (PETM), a prominent paleo-global warming event. Despite the lower nutrient (lower NiEF, CuEF, and ZnEF) contents, and invariable salinity, pH, and light conditions, the PETM interval shows extensive growth of coralline red algae in the hypoxic-oxic water column. Based on these observations, and inferences drawn from the previous laboratory experiments, conducted on the algal growth in varying pCO2 by others, we postulate that the increased atmospheric CO2 concentrations during the PETM probably enhanced the primary productivity of the oligotrophic Tethyan coastal ocean. If so, then the oligotrophic coastal ocean may be considered as an effective CO2 sink and likely to play a pivotal role in carbon cycle-climate connection studies.
... In the oceanic science community, these devices are often employed during the growth of phytoplankton cell cultures to provide a cell count capable of tracking the growth of the cell population. 2,3 Although it has long been recognized that such Coulter Counters can provide quantitative information about the particle dimensions, 4 when it comes to irregularly shaped materials, precisely and accurately relating the measured "equivalent spherical diameter" directly to the mass or volume of the material is not straightforward. 5 Specifically, in terms of ocean science, the amount of calcite produced by individual coccolithophores is an important parameter for the biogeochemical cycle of carbon but is an experimentally challenging measurement. ...
... Assuming that the dissolution rate, J Dis (mol s −1 ), is firstorder with respect to the acid concentration = J kC (mol s ) 1 Dis bulk (2) where k (m 3 s −1 ) is some, as of yet, unknown rate constant and C bulk is the bulk concentration of acetic acid, such that = kM C t mass w bulk dis (3) where t dis is the time taken for the reaction to occur, M w is the molecular weight of the solid (100.1 g mol −1 for calcite), and mass is the calcite mass on a cell. On rearranging eq 3, we get . ...
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Although, in principle, the Coulter Counter technique yields an absolute measure of particle volume, in practice, calibration is near-universally employed. For regularly shaped and non-biological samples, the use of latex beads for calibration can provide sufficient accuracy. However, this is not the case with particles encased in biogenically formed calcite. To date, there has been no effective route by which a Coulter Counter can be calibrated to enable the calcification of coccolithophores─single cells encrusted with biogenic calcite─to be quantified. Consequently, herein, we seek to answer the following question: to what extent can a Coulter Counter be used to provide accurate information regarding the calcite content of a single-species coccolithophore population? Through the development of a new calibration methodology, based on the measurement and dynamic tracking of the acid-driven calcite dissolution reaction, a route by which the cellular calcite content can be determined is presented. This new method allows, for the first time, a Coulter Counter to be used to yield an absolute measurement of the amount of calcite per cell.
... Lipid content is also an important indicator of the nutritional quality of coccolithophores for secondary consumers (Pond and Harris 1996), as also seen for diatoms in particular, and plankton in general (Rossoll et al. 2012;Meyers et al. 2019). Although we see greater availability of E. huxleyi in terms of the production potential of lipids (Fig. 3F), given that the availability of nitrogen under both ocean acidification and warming will be reduced (Fig. 4A), the quality of coccolithophores as a food source will likely be negatively impacted (Conde-Porcuna et al. 2002;Mitra and Flynn 2005;Iglesias-Rodriguez et al. 2008). However, as cellular lipid content is predicted to either be unaffected (Fiorini et al. 2010) or increase under ocean acidification conditions, as is the case here ( Fig. 2A), the nutritional impacts on coccolithophore consumers will likely be varied. ...
... ,B,F,E). Growth rate, for instance, shows a somewhat atypical increase at 20 C(Iglesias- Rodriguez et al. 2008; Langer et al. 2009-morphotypes A, B, R; ...
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Coccolithophores are a calcifying unicellular phytoplankton group that are at the base of the marine food web, and their lipid content provides a source of energy to consumers. Coccolithophores are vulnerable to ocean acidification and warming, therefore it is critical to establish the effects of climate change on these significant marine primary producers, and determine potential consequences that these changes can have on their consumers. Here, we quantified the impact of changes in pH and temperature on the nutritional condition (lipid content, particulate organic carbon/nitrogen), growth rate, and morphology of the most abundant living coccolithophore species, Emiliania huxleyi. We used a regression type approach with nine pH levels (ranging from 7.66 to 8.44) and two temperatures (15°C and 20°C). Lipid production was greater under reduced pH, and growth rates were distinctly lower at 15°C than at 20°C. The production potential of lipids, which estimates the availability of lipids to consumers, increased under 20°C, but decreased under low pH. The results indicate that, while consumers will benefit energetically under ocean warming, this benefit will be mitigated by ocean acidification. The carbon to nitrogen ratio was higher at 20°C and low pH, indicating that the nutritional quality of coccolithophores for consumers will decline under climate change. The impact of low pH on the structural integrity of the coccosphere may also mean that coccolithophores are easier to digest for consumers. Many responses suggest cellular stress, indicating that increases in temperature and reductions in pH may have a negative impact on the ecophysiology of coccolithophores.
... Therefore, the aragonite saturation state (Ω arag ) is also commonly used to assess the impact of ocean acidification on calcareous organisms. The oceanic uptake of anthropogenic CO 2 would result in concomitant changes in seawater chemistry and adverse consequences for many organisms (Gattuso et al., 1999;Langdon and Atkinson, 2005;Iglesias-Rodriguez et al., 2008). Although pH and Ω arag are two commonly used parameters in assessing the impact of ocean acidification, factors (e.g., temperature, CO 2 gas exchange) affecting the distributions of pH and Ω arag could be quite different (Cai et al., 2020). ...
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The problem of ocean acidification caused by the increase of atmospheric carbon dioxide concentration is becoming increasingly prominent. Field observation in the northwest Pacific Ocean was carried out along the 150°E transect in November 2019. The distribution characteristics and influencing factors of the surface seawater carbonate chemistry, including dissolved inorganic carbon (DIC), total alkalinity (TA), pH, partial pressure of carbon dioxide (pCO2) and aragonite saturation state (Ωarag) were investigated. DIC and TA ranged from 1915 to 2014 µmol kg−1 and 2243 to 2291 µmol kg−1, respectively; DIC in general decreased with decreasing latitude, but TA had no clear latitudinal gradient. pCO2 values increased with the decrease of latitude and were all below the atmospheric pCO2 level, ranging from 332 to 387 µatm. pH on the total hydrogen ion concentration scale (pHT) decreased with the decrease of latitude in the range of 8.044–8.110, while Ωarag increased with the decrease of latitude in the range of 2.61–3.88, suggesting that the spatial distributions of pHT and Ωarag were out of phase. Compared with the present, the predicted values of pHT and Ωarag by the end of this century would decrease remarkedly; larger declines were found in the higher pHT and Ωarag regions, resulting in the differences along the meridional gradient becoming smaller for both pHT and Ωarag.
... However, it has been recently demonstrated that the calcification of various calcifying organisms may cause different responses to ocean acidification and other environmental parameter changes (Guinotte and Fabry, 2008;Ries et al., 2009). Moreover, some species of coccolithophores and foraminifera even exhibited enhanced calcification alongside ocean acidification (Iglesias-Rodriguez et al., 2008;Fujita et al., 2011). ...
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Neogloboquadrina pachyderma (sinistral), the dominant planktonic foraminiferal species in the mid-to-high latitude oceans, represents a major component of local calcium carbonate (CaCO3) production. However, the predominant factors, governing the calcification of this species and its potential response to the future marine environmental changes, are poorly understood. The present study utilized an improved cleaning method for the size-normalized weight (SNW) measurement to estimate the SNW of N. pachyderma (sin.) in surface sediments from the Amundsen Sea, the Ross Sea, and the Prydz Bay in the Antarctic Zone of the Southern Ocean. It was found that SNW of N. pachyderma (sin.) is not controlled by deep-water carbonate dissolution post-mortem, and can be therefore, used to reflect the degree of calcification. The comparison between N. pachyderma (sin.) SNW and environmental parameters (temperature, salinity, nutrient concentration, and carbonate system) in the calcification depth revealed that N. pachyderma (sin.) SNWs in the size ranges of 200–250, 250–300, and 300–355 µm are significantly and positively correlated with seawater temperature. Moreover, SNW would increase by ∼30% per degree increase in temperature, thereby suggesting that the calcification of N. pachyderma (sin.) in the modern Antarctic Zone of the Southern Ocean is mainly controlled by temperature, rather than by other environmental parameters such as ocean acidification. Importantly, a potential increase in calcification of N. pachyderma (sin.) in the Antarctic Zone to produce CaCO3 will release CO2 into the atmosphere. In turn, the future ocean warming will weaken the ocean carbon sink, thereby generating positive feedback for global warming.
... In addition, as atmospheric carbon dioxide partial pressure continues to rise, so does uptake of CO 2 into seawater, which reduces seawater pH (pH SW ) and calcium carbonate saturation state (Ω), thereby making seawater less chemically favorable for organisms that produce CaCO 3 shells and skeletons [3]. However, it is understood that some species of marine calcifying organisms are resilient to external acidification or may even benefit by utilizing the additional dissolved inorganic carbon (DIC) available for shell building, and in some cases photosynthesis [4][5][6][7]. ...
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It is thought that the active physiological regulation of the chemistry of a parent fluid is an important process in the biomineralization of scleractinian corals. Biological regulation of calcification fluid pH (pHCF) and other carbonate chemistry parameters ([CO32−]CF, DICCF, and ΩCF) may be challenged by CO2 driven acidification and temperature. Here, we examine the combined influence of changing temperature and CO2 on calcifying fluid regulation in four common Caribbean coral species—Porites astreoides, Pseudodiploria strigosa, Undaria tenuifolia, and Siderastrea siderea. We utilize skeletal boron geochemistry (B/Ca and δ11B) to probe the pHCF, [CO32−]CF, and DICCF regulation in these corals, and δ13C to track changes in the sources of carbon for calcification. Temperature was found to not influence pHCF regulation across all pCO2 treatments in these corals, in contrast to recent studies on Indo-Pacific pocilloporid corals. We find that [DIC]CF is significantly lower at higher temperatures in all the corals, and that the higher temperature was associated with depletion of host energy reserves, suggesting [DIC]CF reductions may result from reduced input of respired CO2 to the DIC pool for calcification. In addition, δ13C data suggest that under high temperature and CO2 conditions, algal symbiont photosynthesis continues to influence the calcification pool and is associated with low [DIC]CF in P. strigosa and P. astreoides. In P. astreoides this effect is also associated with an increase in chlorophyll a concentration in coral tissues at higher temperatures. These observations collectively support the assertion that physicochemical control over coral calcifying fluid chemistry is coupled to host and symbiont physiological responses to environmental change, and reveals interspecific differences in the extent and nature of this coupling.
... The coccolithophore Emiliania huxleyi frequently forms large oceanic algal blooms in subpolar waters, which are significant contributors to the global production and export of calcium carbonate (calcite) [1][2][3]. The collapse of massive E. huxleyi blooms is frequently terminated by the infection of a specific large double-stranded DNA (dsDNA) virus (E. ...
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... The effects of increased pCO 2 concentrations on phytoplankton are not well known. While some studies have reported negative (Gao and Zheng, 2010;Rokitta and Rost, 2012) or neutral (Tortell and Morel, 2002;Feng et al., 2009) responses in primary production, several cultural experiments with recent phytoplankton show an enhanced primary production under elevated CO 2 concentrations (Hein and Sand-Jensen, 1997;Riebesell et al., 2007;Iglesias-Rodriguez et al., 2008;Huang et al., 2018). The biodiversity patterns observed herein are roughly correlated to the atmospheric CO 2 curves based on GEOCARB III (Berner and Kothavala, 2001), GEOCARBSULF (Berner, 2006) and proxies (Royer et al., 2004) (Fig. 10). ...
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Samples taken from DSDP sites 552 and 553 on Hatton Drift and site 611 on Gardar Drift in the NE Atlantic Ocean were examined by analyses of carbonate content, coarse fraction amount and composition, fine fraction size and composition, and oxygen isotope ratios. The age of both sections is the mid-Pleistocene, ranging from the end of the Jaramillo Normal Event to the boundary between the Matuyama and Bruhnes epochs (about 0.77-0.96 Ma). Records of this time show a change from a dominance of 23 ka to longer periodicity at about 0.818 Ma. The grain size is mainly controlled by coccoliths, foraminifera and ice-rafted material, all of which are related to glacial-interglacial changes. Zones barren of and abundant in coccoliths are sensitive indicators of climatic effect. -from Authors
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Two morphotypes of Emiliania huxleyi (Lohmann 1902) Hay et al. 1967, types A and B, known to be unequally distributed in the oceans, were grown in dilution cultures at a range of photon flux densities (PFDs) (1.5–155 μmol photons·m−2·s−1) and two temperatures (10° and 15° C). Calcite carbon and organic carbon content of the cells as well as instantaneous growth rate, cell size, chlorophyll fluorescence, and light-scatter properties clearly depended on growth conditions and differed considerably for the two morphotypes. The ratio between calcite carbon and organic carbon production showed an optimum of 0.65 in E. huxleyi type A cells at PFD = 17.5. The ratio increased slightly with a temperature increase from 10° to 15°C but remained < 1.0 at both temperatures in light-limited cells. In contrast, calcite carbon production exceeded organic carbon production (ratio: 1.4–2.2) in phosphate-deprived cultures. Emiliania huxleyi type B generally showed a higher calcite carbon/organic carbon ratio than E. huxleyi type A, but the relation with PFD was similar. The content of calcite carbon and organic carbon as well as the instantaneous growth rate, cell size, chlorophyll fluorescence, and light-scatter properties showed large diel variations that were closely related to the division cycle. Our results show the importance of mapping the structure of any sampled cell population with respect to the phase in the cell division cycle, as this largely determines the outcome of not only “per cell” measurements but also short time (less than 24 h) flux measurements. For instance, dark production of calcite by E. huxleyi was negatively affected by cell division. Slowly growing (phosphate-stressed) cultures produced calcite in the light and in the dark. In contrast, rapidly growing cultures at 10°C produced calcite only in the light, whereas in the dark there was a significant loss of calcite due to dissolution.