Combined Effects of Photosynthesis and Calcification on the Partial Pressure of Carbon Dioxide in Seawater

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1 Journal of Oceanography, Vol. 54, pp. 1 to 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 ( P CO 2 ) are examined in the light of recent studies and using original model calculations. The ratio of organic carbon to inorganic carbon production (R OI ) determines whether an ecosystem is a net sink or source for atmospheric CO 2. The P CO 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 R OI, the P CO 2 decreases and seawater can absorb atmospheric CO 2. 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. Keywords: Carbon dioxide, photosynthesis, calcification, metabolism, chemical equilibrium, gas exchange, seawater, partial pressure. 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 CO 2 level. The net CO 2 flux between air and sea can be estimated using wind speed, seawater temperature and the difference in the partial pressure of CO 2 between seawater and atmosphere (Bolin, 1960; Broecker and Peng, 1974). Changes in the partial pressure of CO 2 in seawater (P CO2 ) are caused by thermodynamic variations (temperature and salinity), biological activity, and CO 2 exchange with air. The effects of biological activity on P CO2 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 CO 2 in seawater in opposite directions: photosynthesis decreases P CO2 while calcium carbonate production raises P CO2. Calcification tends to drive CO 2 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 CO 2 (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 moles of CO 2 are liberated for each mole of CaCO 3 precipitated in buffered seawater). Frankignoulle et al. (1994) reported that the theoretically predicted Ψ (released CO 2 /precipitated carbonate ratio) is 0.6 when the initial P CO2 is 350 µatm, which confirmed the previous estimates obtained by Ware et al. (1992). Some measurements on calcification and P CO2 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 P CO2, 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 P CO2 are examined quantitatively, according to recent studies and original model calculations. 2. Model Description In order to examine the combined effects of photosynthesis and calcification on the P CO2 in seawater, a model was established using an algorithm originally from Kano (1990) and a modification of Suzuki et al. (1995). To sim- Copyright The Oceanographic Society of Japan. 1

2 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 (CO 2 (aq)* (=H 2 CO 3 + CO 2 (g); total of hydrated and gaseous carbon dioxide), HCO 3, CO 3 2, 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 P CO2 changes caused by metabolism. Main routine (A) and subroutine of iterative method for determining a H (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 A T, a trial value for A C is calculated. Using this A C value and the known value for C T, a new a H value is computed. This new a H value is used to replace the initial trial value for a H 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 a H. This loop is repeated until the difference between the two successive a H 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 a H value is found, the corresponding P CO2 values are computed in the main routine. 2 A. Suzuki

3 [ ] K 1 = a H HCO 3 [ CO 2 ( aq) ], 1 [ ] [ HCO 3 ], 2 K 2 = a H CO 3 2 ( ) [ 4 ] ( ) 3 K B = a H BOH BOH [ ] () ( ), ( 3) K W =[ H + ][ OH ], ( 4) B T = [B(OH) 3 ] + [B(OH) 4 ] = S/35, (5) C T = [CO 2 (aq)*] + [HCO 3 ] + [CO 3 2 ], (6) A T = [HCO 3 ] + 2[CO 3 2 ] + [B(OH) 4 ] + [OH ] [H + ].(7) The concentration is represented by moles of solute per kilogram of seawater (mol kg 1 ) and a H, B T, C T and A T 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 ( f H = a H /[H + ]) is (Peng et al., 1987); the apparent dissociation constants for carbonic acid, bicarbonate ion, boric acid and water (pk 1, pk 2, pk B and pk W ) are 6.002, 9.109, and 13.21, respectively (Millero, 1979). The solubility constant of carbon dioxide in seawater (K H = [CO 2 (aq)*]/p CO2 ) is (Weiss, 1974), and the value of B T is given as a function of salinity (Peng et al., 1987). Organic and inorganic carbon processes in seawater can be represented as changes in C T and A T in this model. Both photosynthesis and calcification lower the C T of seawater, while A T is altered only by the precipitation or dissolution of CaCO 3 (Chisholm and Gattuso, 1991). Calcification lowers the A T by two moles for each mole of CaCO 3 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 P CO2 (δ P CO2 ) using the combination of known C T and A T is illustrated in Fig. 1. Although Skirrow (1965) and Park (1969) proposed approximate solutions for the activity of hydrogen ion (a H ), 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 P CO2 in seawater Figure 2(A) displays changes in P CO2 (δ P CO2 ) 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 P CO2 (δ P CO2 ) caused by the various rates of photosynthesis and calcification. Negative values of carbon production rates indicate respiration and dissolution of CaCO 3. 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 A T, 2000 µmol kg 1 in C T and 25 C in temperature. The corresponding values for P CO2 at S = 35, 20 and 0 were 345 µatm, 222 µatm and 12 µatm, respectively. Shaded area indicates the range of increased P CO2. Effects of Metabolism on Carbon Dioxide in Seawater 3

4 indicates that δ P CO2 depends on the ratio of organic to inorganic production and that P CO2 decreases when the photosynthetic rate is approximately 0.6 times larger than the calcification rate. When the ratio is approximately 0.6, P CO2 apparently does not change from the initial value. P CO2 decreases and atmospheric CO 2 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 CO 2. In the present study, the ratio of organic carbon to inorganic carbon production is defined as R OI and the symbol R 0 OI represents the critical ratio for δ P CO2 = 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 P CO2 are confirmed in Fig. 3, in which P CO2 changes are plotted as a function of reduction in C T. When R OI is equal to 0.60, the P CO2 in seawater is maintained at the initial value. Therefore, R 0 OI is equal to 0.60 for the initial condition of 2000 µmol kg 1 in C T and 345 µatm in P CO2 which roughly corresponds to that of average surface seawater in the early 1990s. In case of higher R OI, the P CO2 in seawater decreases and seawater can absorb atmospheric CO 2. The critical ratio R 0 OI is robust to salinity, while the magnitude of P CO2 changes depends strongly on salinity (Fig. 2). In contrast, the critical ratio R 0 OI is sensitive to the initial condition of the CO 2 system parameters, such as P CO2. The magnitude of P CO2 changes is strongly influenced not only by the biological activity but also by the initial P CO2 value. The CaCO 3 precipitation of 10 µmol kg 1 results in an increase in P CO2 of up to 49.0 µatm at P CO2 = 1000 µatm compared to only 7.4 µatm at P CO2 = 300 µ m under an initial condition of 2400 µmol kg 1 in A T. This result is analogous to those of a previous study obtained by buffer factor examination (Frankignoulle et al., 1994). Photosynthetic effects on P CO2 changes also depend on the initial P CO2 level; a carbon removal of 10 µmol kg 1 results in a P CO2 decrease of 58.0 µatm at P CO2 = 1000 µatm and 12.5 µatm at P CO2 = 3 00 µatm under the same initial conditions. Since P CO2 changes for both photosynthesis and calcification depend on the initial P CO2 condition, the critical ratio R 0 OI also shows a remarkable dependency on the initial P CO2 (Fig. 4). By employing R OI as an indicator of sink-source behavior for atmospheric CO 2, particular attention is needed to distinguish the conditions under which metabolism occurs. Fig. 3. The combined effects of photosynthesis and calcification on P CO2 in seawater at 25 C and S = 35. The initial condition is 345 µatm in P CO2 and µmol kg 1 in C T and corresponding A T is 2346 µmol kg 1. When the ratio of photosynthesis to calcification (R OI ) is equal to 0.60, the P CO2 in seawater is retained as the initial value. In case of higher R OI, the P CO2 in seawater decreases, and hence seawater can absorb atmospheric CO 2. This style of diagram originated with Kano (1990). Fig. 4. The ratio of organic carbon to inorganic carbon production for δ P CO2 = 0 (R OI 0 ) shown as a function of the initial P CO2 in seawater. The results are for seawater with a salinity of 35 at 25 C. The initial condition of seawater is 2346 µmol kg 1 in A T. Shaded area indicates the range of in creased P CO2. 4 A. Suzuki

5 For example, a calcifying plant whose R OI is 0.60 is a potential sink of atmospheric CO 2 under the initial P CO2 condition below 345 µatm. However, the same metabolism may result in a release of CO 2 to the atmosphere when P CO2 of ambient seawater is 800 µatm (Fig. 4). 3.2 Relationship between parameters R OI and Ψ The 0.6 rule (Ware et al., 1992) and Ψ (Frankignoulle et al., 1994) represent molar ratios of released CO 2 to precipitated CaCO 3. On the other hand, R OI is the molar ratio of organic to calcium carbonate production. However, the critical ratio R 0 OI has an identical value to Ψ and displays a similar dependency on salinity and the initial P CO2 in seawater. The degassing and absorption processes of CO 2 in seawater are identical to photosynthetic CO 2 uptake from seawater and respiratory CO 2 release, respectively, considering the effects on the chemical equilibrium in seawater. The gas exchange of CO 2 between air and seawater does not alter A T like organic carbon production processes, while both processes change C T. These indicate that the 0.6 rule proposed for the relationship between CO 2 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 CO 2 from seawater with CaCO 3 precipitation in order to calculate the Ψ value. However, the net CO 2 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 CO 2 + photosynthetic CO 2 uptake)/(precipitated carbonate ratio). Since the air-sea CO 2 exchange is usually a slow reaction compared to metabolism (Marsh and Smith, 1978; Suzuki, 1994), the new definition becomes quite similar to that of R OI. It is inadequate to ignore organic carbon processes in the photo-calcifying system, discussing the relation between the amount of released CO 2 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 P CO2, 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 CaCO 3 supersaturation and carbonate precipitation is enhanced. On the other hand, trans-calcification is induced through the use of active transport mechanisms; an ATP driven Ca 2+ efflux and 2H + uptake create a Ca 2+ rich, alkaline extracytosolic solution, which absorbs CO 2 from the cells and precipitates CaCO 3 (McConnaughey and Falk, 1991). Trans-calcification generates protons, which are used to convert HCO 3 to molecular CO 2, 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 P CO2 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 CaCO 3 supersaturation; photosynthetic CO 2 removal (ciscalcification) or an active Ca 2+ /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 P CO2. Photosynthesis has far less effect on ph and P CO2, 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 R 0 OI 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

6 3.4 Asymmetrical effects of metabolism on P CO2 in seawater Several unique properties of marine metabolism are revealed by the above examination. First, the decreasing effects of photosynthesis on P CO2 are suppressed under low P CO2 conditions, while respiratory P CO2 increase is enhanced under high P CO2 conditions. For example, a carbon addition of 200 µmol kg 1 to seawater with 2000 µmol kg 1 in C T and 345 µatm in P CO2 (the corresponding ph = 8.25) increases P CO2 up to 974 µatm (ph = 7.87), while the same amount of photosynthesis decreases to only 149 µatm in P CO2 (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, CO 2 release from seawater caused by animal respiration precedes CO 2 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 CO 2 transfer is proportional to the difference in the partial pressure of CO 2 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 CO 2 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 P CO2 correspond to 25 C and S = 35. Organic and inorganic processes have vector properties on the A T -C T diagram. Each vector diagram denotes the direction of compositional changes accompanying 200 µmol kg 1 of the indicated process. recognized using an A T vs. C T diagram, originally proposed by Deffeyes (1965), in which corresponding contours of P CO2 are drawn (Fig. 5). Seawater may be a medium which is liable to easily release CO 2 into the atmosphere. The advantage of employing R 0 OI as the criterion governing whether certain aquatic systems act as a source or sink of atmospheric CO 2 has been shown, although there may be several limitations, such as the relatively strong dependency of R 0 OI on the initial P CO2 level. Furthermore, air-sea CO 2 flux integration may provide somewhat different results from examinations using R 0 OI. Some characteristics and rules relating for the R 0 OI criterion basically depend on the thermodynamic equilibrium and not on the dynamic equilibrium. However, R OI 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 In Coral Reefs, Ecosystem of the World 25, ed. by Z. Dubinsky, Elsevier, Amsterdam. Berger, W. H. (1982a): Deglacial CO 2 buildup: constraints on the coral-reef model. Paleogeogr. Paleoclimatol. Paleoecol., 40, Berger, W. H. (1982b): Increase of carbon dioxide in the atmosphere during deglaciation: the coral reef hypothesis. Naturwissenschaften, 69, Bolin, B. (1960): On the exchange of carbon dioxide between the atmosphere and the sea. Tellus, 12, Broecker, W. S. and T.-H. Peng (1974): Gas exchange rates between air and sea. Tellus, 26, 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, Deffeyes, K. S. (1965): Carbonate equilibria: a graphic and algebraic approach. Limnol. Oceanogr., 10, Frankignoulle, M. and J.-P. Gattuso (1993): Air-sea CO 2 exchanges in coastal ecosystems. p In Interactions of the Carbon, Nitrogen, Phosphorus and Sulfur Biogeochemical Cycles and Global Change, NATO ASI Series Vol. 5, ed. by 6 A. Suzuki

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