Journal of Oceanography, Vol. 54, pp. 1 to 7. 1998
Combined Effects of Photosynthesis and Calcification on
the Partial Pressure of Carbon Dioxide in Seawater
ATSUSHI SUZUKI
Marine Geology Department, Geological Survey of Japan, Tsukuba 305, Japan; and
Australian Institute of Marine Science, Townsville, Queensland, 4810, Australia
(Received 13 September 1996; in revised form 24 July 1997; accepted 24 July 1997)
The effects of marine photosynthesis and calcification on the partial pressure of carbon
dioxide in seawater ( PCO 2 ) are examined in the light of recent studies and using original
model calculations. The ratio of organic carbon to inorganic carbon production (ROI)
determines whether an ecosystem is a net sink or source for atmospheric CO2. The PCO 2
maintains its initial value when the photosynthetic rate is approximately 0.6 times the
calcification rate under normal sea surface condition. In case of higher ROI, the PCO 2
decreases and seawater can absorb atmospheric CO2 . The ratio of organic carbon to
inorganic carbon production can be used as a potential indicator of sink-source behavior
in aquatic photo-calcifying systems.
bonate ratio) is 0.6 when the initial PCO2 is 350 µatm, which
confirmed the previous estimates obtained by Ware et al.
(1992).
Some measurements on calcification and PCO2 were
made and a discrepancy between observation and model
prediction became evident: observed Ψ = 0.1 at an organism
level for scleractinian coral with zooxanthelle (Frankignoulle
and Gattuso, 1993); Ψ = 0.06 at a community level (Gattuso
et al., 1993). These large differences are attributed mainly to
a tight coupling between photosynthesis and calcification
(Frankignoulle et al., 1994). Kayanne et al. (1995) reported
that a fringing reef in the Ryukyus has a decreasing effect on
PCO2 , in spite of its rapid calcification. This may also be
attributed to a tight coupling between organic and inorganic
carbon metabolism. Kano (1990) proposed the coupled
model of photosynthesis and calcification and his model is
useful for understanding a tight coupling between organic
and inorganic carbon processes.
Further consideration of the coupled conditions of
organic and inorganic carbon process is essential in order to
ascertain the role of the marine calcifying system. In the
present study, the combined effects of marine photosynthesis
and calcification on PCO2 are examined quantitatively, according to recent studies and original model calculations.
1. Introduction
The role of the oceans in the global carbon cycle is a
subject of contention in respect of their role in the maintenance of the atmospheric CO2 level. The net CO2 flux between air and sea can be estimated using wind speed,
seawater temperature and the difference in the partial pressure
of CO2 between seawater and atmosphere (Bolin, 1960;
Broecker and Peng, 1974). Changes in the partial pressure of
CO2 in seawater ( PCO2 ) are caused by thermodynamic
variations (temperature and salinity), biological activity,
and CO2 exchange with air. The effects of biological activity
on PCO2 have received less attention than the thermodynamic
effects (e.g. Weiss et al., 1982; Takahashi et al., 1993).
Marine photosynthesis and calcification shift the
chemical equilibrium of CO2 in seawater in opposite directions: photosynthesis decreases PCO2 while calcium carbonate production raises PCO2 . Calcification tends to drive
CO2 from the ocean to the atmosphere, although it consumes
carbonate and/or bicarbonate ions. This paradox has become
well understood due to many enlightening papers (Kano,
1990; Ware et al., 1992; Frankignoulle et al., 1994; Suzuki,
1994; Frankignoulle et al., 1995). Some models have been
proposed in which a calcifying system such as a coral reef
acts as a source of atmospheric CO2 (Berger, 1982a, b;
Opdyke and Walker, 1992).
The “0.6 rule” was proposed by Ware et al. (1992) using
a simple chemical equilibrium model (i.e. 0.62 moles of CO2
are liberated for each mole of CaCO3 precipitated in buffered seawater). Frankignoulle et al. (1994) reported that the
theoretically predicted Ψ (released CO2/precipitated car-
2. Model Description
In order to examine the combined effects of photosynthesis and calcification on the PCO2 in seawater, a model
was established using an algorithm originally from Kano
(1990) and a modification of Suzuki et al. (1995). To sim-
1
Copyright  The Oceanographic Society of Japan.
Keywords:
⋅ Carbon dioxide,
⋅ photosynthesis,
⋅ calcification,
⋅ metabolism,
⋅ chemical equilibrium,
⋅ gas exchange,
⋅ seawater,
⋅ partial pressure.
plify the treatment of carbonate equilibrium in seawater, I
consider a control mass of seawater closed to the atmosphere.
This control mass is under a pressure of one atmosphere.
Consideration of seven solute components is required
(CO2(aq)* (=H2CO3 + CO2(g); total of hydrated and gaseous carbon dioxide), HCO3– , CO32–, H+ , OH–, B(OH)3 and
B(OH)4–) in order to make an exact algebraic calculation of
the carbonate equilibrium system in seawater. This system
can be described completely using a system of seven simultaneous equations with respect to the concentrations of
solute components. The set of equations consists of four
equations describing equilibrium relationships (Eqs. (1) to
(4)), two concentration conditions (Eqs. (5) and (6)) and one
condition stating the electroneutrality of the solution (Eq.
(7)). These equations can be written as follows (Stumm and
Morgan, 1981):
Fig. 1. Flow charts of the model for calculating PCO2 changes caused by metabolism. Main routine (A) and subroutine of iterative
method for determining aH (activity of hydrogen ion) following Peng et al. (1987) (B) are shown. In the iterative subroutine, an
initial trial value of a H is first used to compute the values of [H+], [OH– ] and [B(OH)4–]. Subtracting these values from the known
value of AT , a trial value for AC is calculated. Using this AC value and the known value for CT, a new aH value is computed. This
new aH value is used to replace the initial trial value for aH in the first step, and to compute refined values for [H+], [OH–] and [B
(OH)4– ]. These values are then used to compute a refined value for aH. This loop is repeated until the difference between the two
successive aH values is reduced to less than 0.005%. This type of iterative scheme always yields a stable solution, and it generally
takes less than 10 iterations to achieve this level of convergence (Peng et al., 1987). Once a stable aH value is found, the corresponding PCO2 values are computed in the main routine.
2
A. Suzuki
K1 ′ =
[
],
(1)
],
(2)
aH HCO 3−
[CO (aq ) ]
∗
2
K2 ′ =
KB ′ =
[
aH CO 32 −
[
HCO 3−
]
[
−
[ ][
]
aH B( OH ) 4
[B(OH)3 ]
],
(3)
K W ′ = H + OH − ,
( 4)
BT = [B(OH)3] + [B(OH)4 –] = 4.106 × 10–4S/35,
(5)
CT = [CO2(aq)*] + [HCO3–] + [CO32–],
(6)
AT = [HCO3– ] + 2[CO32–] + [B(OH)4–] + [OH– ] – [H+ ].(7)
The concentration is represented by moles of solute per
kilogram of seawater (mol kg–1) and aH, BT, CT and AT are
hydrogen ion activity, total boron, total dissolved inorganic
carbon (total carbon dioxide) and total alkalinity, respectively. Values of constants and coefficients based on the
NBS buffer scale used in this model calculations at 25°C and
S = 35 are as follows: the apparent total hydrogen ion
activity coefficient ( fH = aH/[H+]) is 0.704 (Peng et al., 1987);
the apparent dissociation constants for carbonic acid, bicarbonate ion, boric acid and water (pK1′, pK2 ′, pKB′ and pKW ′)
are 6.002, 9.109, 8.692 and 13.21, respectively (Millero,
1979). The solubility constant of carbon dioxide in seawater
(KH′ = [CO2(aq)*]/ PCO2 ) is 0.02839 (Weiss, 1974), and the
value of BT is given as a function of salinity (Peng et al., 1987).
Organic and inorganic carbon processes in seawater
can be represented as changes in CT and AT in this model.
Both photosynthesis and calcification lower the CT of seawater, while AT is altered only by the precipitation or dissolution of CaCO3 (Chisholm and Gattuso, 1991). Calcification lowers the AT by two moles for each mole of CaCO3
precipitated. These relationships are independent of the
carbon species used for photosynthesis and calcification
(Smith and Key, 1975).
The procedure for calculating the difference in initial
and altered PCO2 (δ PCO2 ) using the combination of known
CT and AT is illustrated in Fig. 1. Although Skirrow (1965)
and Park (1969) proposed approximate solutions for the
activity of hydrogen ion (aH), the exact one is preferred,
found by using the iterative method described by Peng et al.
(1987). Details of calculation procedures are described in
the appendices of Suzuki et al. (1995) and Peng et al. (1987).
3. Model Results and Discussion
3.1 Critical ratio for unchanged PCO2 in seawater
Figure 2(A) displays changes in PCO2 (δ PCO2 ) caused
by various combinations of organic and inorganic production in seawater with a salinity of 35 at 25°C. This figure
Fig. 2. Changes in PCO2 (δ PCO2 ) caused by the various rates of photosynthesis and calcification. Negative values of carbon production
rates indicate respiration and dissolution of CaCO3 . Calculations are conducted for three salinity conditions (S = 35 (A), 20 (B) and
0 (C)) and supposing initial condition of seawater is 2346 µmol kg –1 in AT , 2000 µmol kg –1 in CT and 25°C in temperature. The
corresponding values for PCO2 at S = 35, 20 and 0 were 345 µatm, 222 µatm and 12 µatm, respectively. Shaded area indicates the
range of increased PCO2 .
Effects of Metabolism on Carbon Dioxide in Seawater
3
indicates that δ PCO2 depends on the ratio of organic to
inorganic production and that PCO2 decreases when the
photosynthetic rate is approximately 0.6 times larger than
the calcification rate. When the ratio is approximately 0.6,
PCO2 apparently does not change from the initial value. PCO2
decreases and atmospheric CO2 is consequently absorbed
into seawater when the photosynthetic rate is larger than this
boundary. This is the criterion that governs whether a reef
community acts as a sink or source for atmospheric CO2. In
the present study, the ratio of organic carbon to inorganic
carbon production is defined as ROI and the symbol ROI0
represents the critical ratio for δ PCO2 = 0. The critical value
of 0.6 is quite similar to those proposed by Ware et al. (1992)
and Frankignoulle et al. (1994). The relationship between
these values will be discussed later.
The combined effects of photosynthesis and calcification on PCO2 are confirmed in Fig. 3, in which PCO2 changes
are plotted as a function of reduction in CT. When ROI is equal
Fig. 3. The combined effects of photosynthesis and calcification
on PCO2 in seawater at 25°C and S = 35. The initial condition
is 345 µatm in PCO2 and 2 000 µmol kg–1 in CT and corresponding AT is 2346 µmol kg –1. When the ratio of photosynthesis to calcification (ROI) is equal to 0.60, the PCO2 in seawater is retained as the initial value. In case of higher ROI, the
PCO2 in seawater decreases, and hence seawater can absorb
atmospheric CO2. This style of diagram originated with Kano
(1990).
4
A. Suzuki
to 0.60, the PCO2 in seawater is maintained at the initial
value. Therefore, ROI0 is equal to 0.60 for the initial condition of 2000 µmol kg–1 in CT and 345 µatm in PCO2 which
roughly corresponds to that of average surface seawater in
the early 1990s. In case of higher ROI, the PCO2 in seawater
decreases and seawater can absorb atmospheric CO2.
The critical ratio ROI0 is robust to salinity, while the
magnitude of PCO2 changes depends strongly on salinity
(Fig. 2). In contrast, the critical ratio ROI 0 is sensitive to the
initial condition of the CO2 system parameters, such as PCO2 .
The magnitude of PCO2 changes is strongly influenced not
only by the biological activity but also by the initial PCO2
value.
The CaCO3 precipitation of 10 µmol kg–1 results in an
increase in PCO2 of up to 49.0 µatm at PCO2 = 1000 µatm
compared to only 7.4 µatm at PCO2 = 300 µ m under an initial
condition of 2400 µmol kg–1 in AT. This result is analogous
to those of a previous study obtained by buffer factor
examination (Frankignoulle et al., 1994). Photosynthetic
effects on PCO2 changes also depend on the initial PCO2
level; a carbon removal of 10 µmol kg–1 results in a PCO2
decrease of 58.0 µatm at PCO2 = 1000 µatm and 12.5 µatm
at PCO2 = 3 00 µatm under the same initial conditions. Since
PCO2 changes for both photosynthesis and calcification
depend on the initial PCO2 condition, the critical ratio ROI0
also shows a remarkable dependency on the initial PCO2
(Fig. 4). By employing ROI as an indicator of sink-source
behavior for atmospheric CO2, particular attention is needed
to distinguish the conditions under which metabolism occurs.
Fig. 4. The ratio of organic carbon to inorganic carbon production
for δ PCO2 = 0 (ROI0) shown as a function of the initial PCO2 in
seawater. The results are for seawater with a salinity of 35 at
25°C. The initial condition of seawater is 2346 µ mol kg–1 in
AT . Shaded area indicates the range of in creased PCO2 .
For example, a calcifying plant whose ROI is 0.60 is a potential sink of atmospheric CO2 under the initial PCO2
condition below 345 µatm. However, the same metabolism
may result in a release of CO2 to the atmosphere when PCO2
of ambient seawater is 800 µatm (Fig. 4).
3.2 Relationship between parameters ROI and Ψ
The “0.6 rule” (Ware et al., 1992) and Ψ (Frankignoulle
et al., 1994) represent molar ratios of released CO2 to precipitated CaCO3. On the other hand, ROI is the molar ratio of
organic to calcium carbonate production. However, the
critical ratio ROI0 has an identical value to Ψ and displays a
similar dependency on salinity and the initial PCO2 in seawater. The degassing and absorption processes of CO2 in
seawater are identical to photosynthetic CO2 uptake from
seawater and respiratory CO2 release, respectively, considering the effects on the chemical equilibrium in seawater.
The gas exchange of CO2 between air and seawater does not
alter AT like organic carbon production processes, while
both processes change CT. These indicate that the “0.6 rule”
proposed for the relationship between CO2 released and
calcium carbonate precipitation is applicable to the relationship between photosynthetic carbon removal and calcification.
From this view point, another interpretation can be
proposed to explain the large discrepancy between observations and model predictions reported by Frankignoulle and
Gattuso (1993) and Gattuso et al. (1993). They compared
the amount of directly measured flux of CO2 from seawater
with CaCO3 precipitation in order to calculate the Ψ value.
However, the net CO2 change due to organic carbon process
must also be taken into account. In applying the Ψ concept
to tank experiments or field observations, the definition of
Ψ should be changed as follows: Ψ = (released CO2 +
photosynthetic CO2 uptake)/(precipitated carbonate ratio).
Since the air-sea CO2 exchange is usually a slow reaction
compared to metabolism (Marsh and Smith, 1978; Suzuki,
1994), the new definition becomes quite similar to that of
ROI. It is inadequate to ignore organic carbon processes in
the “photo-calcifying” system, discussing the relation between the amount of released CO2 and precipitated carbonate.
3.3 Functional linkage between calcification and photosynthesis
It is a well known phenomenon that the calcification of
marine plants and algae-invertebrate symbioses is stimulated
by photosynthesis (Barnes and Chalker, 1990). However, an
alternative functional linkage between calcification and
photosynthesis was recently proposed at the organism level
(McConnaughey, 1991) and the community level (Suzuki et
al., 1995). These studies examined the ability of calcification to raise aquatic PCO2 , which has potentially positive
effects on photosynthesis. McConnaughey (1994) described
two kinds of functional association between calcification
and photosynthesis: “cis” calcification and “trans” calcification. Cis-calcification is induced by photosynthetic carbon uptake under control of the carbonate equilibrium;
carbon removal for photosynthesis results in CaCO3 supersaturation and carbonate precipitation is enhanced. On
the other hand, trans-calcification is induced through the use
of active transport mechanisms; an ATP driven Ca2+ efflux
and 2H+ uptake create a Ca2+ rich, alkaline extracytosolic
solution, which absorbs CO2 from the cells and precipitates
CaCO3 (McConnaughey and Falk, 1991). Trans-calcification
generates protons, which are used to convert HCO3 – to
molecular CO2 , and allows more efficient carbon withdrawals to be made from mildly alkaline, calcium rich
waters (such as the oceans) than does cis-calcification
(McConnaughey, 1994).
According to the hypothesis of McConnaughey (1994),
the maximum optimized photosynthesis would be achieved
in the unchanged PCO2 condition. Therefore, the model in
the present study is applicable to examine the maximum
optimized condition for photosynthesis, regardless of the
calcification mechanism. The carbonate system can be determined by total amounts of photosynthesis and calcification. Model calculations are never affected by the cause of
the CaCO3 supersaturation; photosynthetic CO2 removal (ciscalcification) or an active Ca2+/2H+ exchange (trans-calcification).
McConnaughey (1994) pointed out the 1:1 soichiometry
of calcification to photosynthesis allows carbon withdrawals to be made from freshwater with minimal impact on
PCO2 . Photosynthesis has far less effect on pH and PCO2 , if
combined with an equal amount of calcification.
McConnaughey (1994) stated, without careful analysis, that
an approximately 1:1 ratio is applicable in the marine
calcifying autotrophs. However, the ROI0 criterion is 0.6 for
seawater, thus the maximum condition would be expected
for the approximately 1:0.6 (or 1.7:1) ratio of calcification
to photosynthesis. By an analogous argument, combined
with the “0.6 rule” for seawater, the approximately 1:1 ratio
of calcification to photosynthesis is common in freshwater
(McConnaughey, 1994), so a 1:0.6 ratio may be common for
marine calcifying autotrophs. However, short-term (2–3
hour) incubations of coral reef autotrophs show that photosynthesis is higher than calcification by a factor of 2 to 8
during the daytime (Kinsey, 1985; Barnes and Chalker,
1990) and this result is contrary to expectation. On the other
hand, the tissue ratio of inorganic carbon to organic carbon
in calcifying reef autotrophs seems to be relatively close to
expectation (Zimmerman et al., 1996). A detailed discussion of the calcifying mechanism and photosynthesis/calcification ratio of marine calcifying autotrophs would go
beyond the limitations of this essay and a more careful
analysis will be needed.
Effects of Metabolism on Carbon Dioxide in Seawater
5
3.4 Asymmetrical effects of metabolism on PCO2 in seawater
Several unique properties of marine metabolism are
revealed by the above examination. First, the decreasing
effects of photosynthesis on PCO2 are suppressed under low
PCO2 conditions, while respiratory PCO2 increase is enhanced under high PCO2 conditions. For example, a carbon
addition of 200 µmol kg–1 to seawater with 2000 µmol
kg–1 in CT and 345 µatm in PCO2 (the corresponding pH =
8.25) increases PCO2 up to 974 µatm (pH = 7.87), while the
same amount of photosynthesis decreases to only 149 µatm
in PCO2 (pH = 8.53). Based on this property, the following
argument can be formulated. Assuming that there are plants
and animals in separate seawater tanks open to the atmosphere, CO2 release from seawater caused by animal respiration precedes CO2 invasion due to photosynthesis, even
if production and consumption of the plants and animals are
balanced as a whole. In this argument it is assumed that airsea CO2 transfer is proportional to the difference in the
partial pressure of CO2 between the two phases, and that
other conditions such as temperature and wind speed of both
tanks are similar. This can be recognized in the case of
inorganic carbon processes. Comparable amounts of calcification and dissolution in separate quantities of seawater
with the same initial conditions may result in the net release
of CO2 from the seawater. These features can be visually
Fig. 5. Total alkalinity vs. total carbon dioxide diagram illustrating the effects of photosynthesis, calcification and their reverse
reactions. Contours of PCO2 correspond to 25°C and S = 35.
Organic and inorganic processes have vector properties on the
AT -CT diagram. Each vector diagram denotes the direction of
compositional changes accompanying 200 µmol kg–1 of the
indicated process.
6
A. Suzuki
recognized using an AT vs. CT diagram, originally proposed
by Deffeyes (1965), in which corresponding contours of
PCO2 are drawn (Fig. 5). Seawater may be a medium which
is liable to easily release CO2 into the atmosphere.
The advantage of employing ROI 0 as the criterion governing whether certain aquatic systems act as a source or
sink of atmospheric CO2 has been shown, although there
may be several limitations, such as the relatively strong
dependency of ROI0 on the initial PCO2 level. Furthermore,
air-sea CO2 flux integration may provide somewhat different
results from examinations using ROI0. Some characteristics
and rules relating for the ROI0 criterion basically depend on
the thermodynamic equilibrium and not on the dynamic
equilibrium. However, ROI can be applied as a simple indicator of sink-source behavior to not only reef communities
but also other marine environments such as coccolithophorid
blooms.
Acknowledgements
I am very grateful to Dr. T. Nakamori of Tohoku
University, Dr. H. Kayanne of the University of Tokyo, Dr.
H. Kawahata of the Geological Survey of Japan, Dr. K.
Nozaki of the Electrotechnical Laboratory, and Mr. Steven
Kraines of the University of Tokyo for their valuable suggestions and discussions. Several reviewers made useful
criticisms that significantly improved earlier versions of the
present paper. This work is supported by “R & D for Global
Environmental Technology” of the Agency of Industrial
Science and Technology, Ministry of International Trade
and Industry.
References
Barnes, D. J. and B. E. Chalker (1990): Calcification and photosynthesis in reef-building corals and algae. p. 109–131. In
Coral Reefs, Ecosystem of the World 25, ed. by Z. Dubinsky,
Elsevier, Amsterdam.
Berger, W. H. (1982a): Deglacial CO2 buildup: constraints on the
coral-reef model. Paleogeogr. Paleoclimatol. Paleoecol., 40,
235–253.
Berger, W. H. (1982b): Increase of carbon dioxide in the atmosphere
during deglaciation: the coral reef hypothesis.
Naturwissenschaften, 69, 87–88.
Bolin, B. (1960): On the exchange of carbon dioxide between the
atmosphere and the sea. Tellus, 12, 274–281.
Broecker, W. S. and T.-H. Peng (1974): Gas exchange rates
between air and sea. Tellus, 26, 21–35.
Chisholm, R. M. and J.-P. Gattuso (1991): Validation of the
alkalinity anomaly technique for investigating calcification
and photosynthesis in coral reef communities. Limnol.
Oceanogr., 36, 1232–1239.
Deffeyes, K. S. (1965): Carbonate equilibria: a graphic and
algebraic approach. Limnol. Oceanogr., 10, 412–426.
Frankignoulle, M. and J.-P. Gattuso (1993): Air-sea CO2 exchanges
in coastal ecosystems. p. 233–248. In Interactions of the
Carbon, Nitrogen, Phosphorus and Sulfur Biogeochemical
Cycles and Global Change, NATO ASI Series Vol. 5, ed. by
R. Wollast, F. T. Mackenzie and L. Chou, Springer-Verlag,
Berlin.
Frankignoulle, M., C. Canon and J.-P. Gattuso (1994): Marine
calcification as a source of carbon dioxide: Positive feedback
of increasing atmospheric CO2. Limnol. Oceanogr., 39, 158–
462.
Frankignoulle, M., M. Pichion and J.-P. Gattuso (1995): Aquatic
calcification as a source of carbon dioxide. p. 265–271. In
Carbon Sequestration in the Biosphere, NATO ASI Series,
Vol. 33, ed. by M. A. Beran, Springer-Verlag, Berlin.
Gattuso, J.-P., M. Pichon, B. Delesalle and M. Frankignoulle
(1993): Community metabolism and air-sea CO2 fluxes in a
coral reef ecosystem, (Moorea, French Polynesia). Mar. Ecol.
Prog. Ser., 96, 259–267.
Kano, Y. (1990): Relation between increase of coral and atmospheric carbon dioxide concentration. Umi to Sora, 65, 259–
265 (in Japanese).
Kayanne, H., A. Suzuki and H. Saito (1995): Diurnal changes in
the partial pressure of carbon dioxide coral reef water. Science,
269, 214–216.
Kinsey, D. W. (1985): Metabolism, calcification and carbon
production. I Systems level studies. Proc. 5th Int. Coral Reef
Congr., 4, 505–526.
Marsh, J. A., Jr. and S. V. Smith (1978): Productivity measurements
of coral reefs in flowing water. p. 361–377. In Coral Reefs:
Research Methods, ed. by D. R. Stoddart and R. E. Johannes,
Unesco, Paris.
McConnaughey, T. (1991): Calcification in Chara corallina: CO2
hydroxylation generates protons for bicarbonate assimilation.
Limnol. Oceanogr., 36, 619–628.
McConnaughey, T. (1994): Calcification, photosynthesis, and
global carbon cycles. Bull. de l’Institut Océanographique
Monaco, no spécial 13, 137–161.
McConnaughey, T. A. and R. H. Falk (1991): Calcium-proton
exchange during algal calcification. Biol. Bull., 180, 185–195.
Millero, F. J. (1979): The thermodynamics of the carbonate
system in seawater. Geochim. Cosmochim. Acta, 43, 1651–
1661.
Opdyke, B. N. and J. C. G. Walker (1992): Return of the coral reef
hypothesis: Basin to shelf partitioning of CaCO3 and its effect
on atmospheric CO2. Geology, 20, 733–736.
Park, P. K. (1969): Oceanic CO2 systems: an evaluation of 10
methods of investigation. Limnol. Oceanogr., 14, 179–186.
Peng, T.-H., T. Takahashi, W. S. Broecker and J. Oladsson (1987):
Seasonal variability of carbon dioxide, nutrients and oxygen
in the northern Atlantic surface water: observations and a
model. Tellus, 89B, 439–458.
Skirrow, G. (1965): The dissolved gases—Carbon dioxide. p.
227–322. In Chemical Oceanography, Vol. 1, ed. by J. P.
Riley and G. Skirrow, Academic Press, New York.
Smith, S. V. and G. S. Key (1975): Carbon dioxide and metabolism in marine environments. Limnol. Oceanogr., 20, 439–459.
Stumm, W. and J. J. Morgan (1981): Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Waters. John Wiley & Sons, New York, 780 pp.
Suzuki, A. (1994): Seawater CO2 system and its transformation
caused by photosynthesis and calcification in coral reefs—
theory and measurements of the reef metabolism. Bull. Geol.
Surv. Japan, 45, 573–623 (in Japanese with English abstract).
Suzuki, A., T. Nakamori and H. Kayanne (1995): The mechanism
of production enhancement in coral reef carbonate system:
model and empirical results. Sediment. Geol., 99, 259–280.
Takahashi, T., J. Olafsson, J. G. Goddard, D. W. Chipman and S.
C. Sutherland (1993): Seasonal variation of CO2 and nutrients
in the high-latitude surface oceans: a comparative study.
Global Biogeochem. Cycles, 7, 843–878.
Ware, J. R., S. V. Smith and M. L. Reaka-Kudla (1992): Coral
reefs: sources or sinks of atmospheric CO2 ? Coral Reefs, 11,
127–130.
Weiss, R. F. (1974): Carbon dioxide in water and seawater: The
solubility of a non-ideal gas. Mar. Chem., 2, 203–215.
Weiss, R. F., R. A. Jahnke and C. D. Keeling (1982): Seasonal
effects of temperature and salinity on the partial pressure of
CO2 in seawater. Nature, 300, 511–513.
Zimmerman, R. C., D. L. Steller, J. A. Coyer and, R. S. Alberte
(1996): Photosynthesis and calcification by coral reef autotrophs: Impact on air/sea flux of CO2. p. 216, In Abstracts,
8th Int. Coral Reef Symp., Panama..
Effects of Metabolism on Carbon Dioxide in Seawater
7