REVIEWS OF GEOPHYSICS, SUPPLEMENT, PAGES 1253-1262, JULY 1995 U.S. NATIONAL REPORT TO INTERNATIONAL UNION OF GEODESY AND GEOPHYSICS 1991-1994 The atmospheric oxygen cycle: The oxygen isotopes of atmospheric C02 and 02 and the 02/N2 ratio Ralph F. Keeling Scripps Institution of Oceanography, University of California, San Diego, La Jolla Introduction to come to isotopic equilibrium with liquid water is the same as the time scale for hydration, i.e., around 30 sec­ 18 16 Oxygen is the most abundant element in the earth's onds [Mills and Urey, 1940]. The 0/ 0 ratio of C02 crust, it accounts for 89% of the mass of the ocean, and in equilibrium with water at 25° C is 1.041 times higher 18 16 it is the second most abundant element in the earth's than the 0/ 0 ratio of the water. This equilibrium atmosphere. Much work on the oxygen cycle has fo­ fractionation factor varies slightly with temperature. Isotopic ratios are generally reported according to cused on the question of the origin of atmospheric 02 and its variations over geologic time [see Kump et al, 18 16 18 16 1991, and references therein). This review focuses on S = ( 0/ 0)sampie/( 0/ 0),Wflrd " 1 (1) several other aspects of the oxygen cycle including the short-term controls on the oxygen isotopic abundance where the S value is customarily multiplied by 1000 and expressed in per mille (%<>)• Bottinga and Craig [1969] of atmospheric C02 and 02, and the short-term vari- abilitiy in the 0 /N ratio. suggested using a standard based on CO2 in equilib­ 2 2 rium with the Standard Mean Ocean Water (SMOW) at These aspects of the oxygen cycle depend mainly on 25°C [Craig and Gordon, 1965]. Most recent measure­ material exchanges between the atmosphere and living ments have been reported relative to the 180/160 ra­ organisms at the earth's surface or in the ocean. Like tio of C0 derived from the Pee-Dee Belemnite (PDB) several other atmospheric variables which have received 2 carbonate standard. This standard has an 180/160 ra­ much attention recently, e.g., the abundances of C0 , 2 tio that is 0.22%o higher than the Bottinga and Craig CH4, and N 0, the oxygen isotopic content of C0 and 2 2 standard [Friedman and O'Neil, 1977]. 02 and the 02/N2 ratio have atmospheric lifetimes that 18 16 are long relative to the time scale of atmospheric mix­ The 0/ 0 ratio of atmospheric CO2 is primarily ing and thus reflect an integration of material exchanges determined by exchanges with leaf water, soil water, over the globe. Recently, our knowledge of these vari­ and surface sea water [Francey and Tans, 1987; Far- ables has expanded through laboratory experiments ex­ quhar et al., 1993]. Oxygen atom exchange with leaf water occurs because a significant fraction of the C0 ploring the exchange pathways, and through measure­ 2 ments on contemporary air samples or in ancient air which diffuses into the chloroplasts of leaf cells is not samples extracted from polar ice cores. This review assimilated but diffuses back into the air, and this frac­ summarizes recent literature on these subjects, and also tion will have equilibrated isotopically with chloroplast emphasizes how these aspects of the global oxygen cycle water. Equilibration occurs in spite of the short (< 1 second) residence time of C0 in leaves because of the can provide new information on the material exchanges 2 between the atmosphere and biota integrated over large presence of the enzyme carbonic anhydrase, which is areas. concentrated in the chloroplasts of leaf cells and which dramatically speeds up the hydration reaction. Oxygen atom exchange with soil water occurs primarily through The 180/160 Ratio of Atmospheric C0 2 C02 which is released into the soil by below-ground res­ piration and which subsequently diffuses into the atmo­ The oxygen isotopic content of atmospheric C02 is sphere. Oxygen atom exchange with seawater occurs mainly determined by interactions between C02 and through the exchange of C02 molecules across the air- the global reservoirs of liquid water. This follows be­ sea interface. cause direct gas phase interactions of C02 with 02 and The oxygen isotopic composition of soil water and H20 vapor do not result in O atom exchange [Francey leaf water vary considerably. Soil water isotopic com­ and Tans, 1987]. When C02 dissolves in water, oxy­ position tends to follow the composition of precipitation gen atoms are exchanged through a mechanism that which is progressively depleted in 180 relative to seawa­ involves the hydration of dissolved C02 to form car­ ter towards high latitudes and towards the-interior of bonic acid (H2C03). The time scale for dissolved C02 continents. Chloroplast water, in turn, tends to be en­ riched in 180 relative to soil water by evaporation from leaves because H2160 evaporates preferentially relative Copyright 1995 by the American Geophysical Union. to H2180. This enrichment of chloroplast water is sensi­ tive to relative humidity and temperature, which can be Paper number 95RG00438. highly variable [Dongmann et al., 1974; Forstel, 1978; 8755-1209/95/95RG-00438$15.00 Zundel et al, 1978]. 1253 1254 KEELING: ATMOSPHERIC OXYGEN CYCLE A global steady-state budget for 6lsO of atmospheric is where does chloroplast water fall in this range. Far­ CO2 is shown in Figure 1. This budget uses figures quhar et al. [1993] present results based on isotope ex­ from Farquhar et al [1993] for fluxes and isotopic ex­ change experiments with several varieties of fruit trees changes of atmospheric CO2 with leaf, soil, and sea wa­ that suggest the isotopic composition of chloroplast wa­ ter. One significant source of uncertainty here is the ter is virtually identical to that of water at the evap­ global average isotopic composition of chloroplast wa­ orating surfaces in leaves. The budget in Figure 1 is ter. Logically, the 6lsO of chloroplast water should be based on this assumption, taking into account the vari­ intermediate between that of soil water and water at ability of leaf water over the surface of the earth. In the evaporating surface in the leaves where the max­ contrast, Yakir and coworkers have conducted isotope imum isotopic enrichment occurs. A critical question exchange experiments on sunflowers that indicate that Figure 1. The global "pre-anthropogenic" steady-state budget for the oxygen isotopes of atmo­ spheric CO2 based on Farquhar et al. [1993] showing annual fluxes of CO2 in units of 1015 moles of carbon and showing the isotopic composition of C02 in equilibrium with dominant exchangeable water reservoirs [see also Keeling, 1993]. CO2 exchange with soil water involves uptake of CO2 by leaves, respiration within the soil, and diffusion of the respiratory C02 out through the soil. The budget shown here assumes that the kinetic isotope fractionation that results from diffusion through stomata and through the soil cancel each other out (see also Table 2, Eq. (F)). According to this budget, the bulk composition of atmospheric CO2 can be explained by assuming that 45% of the oxygen atoms come from chloroplast water at an average isotopic composition of -f5%o> 34% come from soil water at an average of — 7%o, and 21% come from sea water at an average of l%o- This combination yields atmospheric CO2 at approximately 0%o- All numbers here are relative to the PDB standard. KEELING: ATMOSPHERIC OXYGEN CYCLE 1255 chloroplast water is typically 6 to 10%o depleted in 180 Table 1. Summarizing Two Alternative Formulations for compared to water at the evaporating surface [Yakir et Describing Exchanges of Oxygen Isotopes of C02 with al, 1993; Yakir et al, 1994]. The difference in 6180 be­ Terrestrial Ecosystems tween chloroplasts and evaporation sites probably varies NOTATION: significantly from species to species [Yakir et al, 1993]. C0 Atmospheric CO2 partial pressure (PCO2) A global model describing oxygen atom exchanges of Cc PCO2 in chloroplast 18 18 ie CO2 with terrestrial ecosystems has been developed by Ca Atmospheric C O O partial pressure Farquhar et al [1993] (see Table 1, Equation G). This 18 16 Ra 0/ 0 ratio of atmospheric C02 model is based on a formulation in which the oxygen- 18 16 Rc 0/ 0 ratio of C02 in equilibrium with chloro­ atom exchanges with leaf water are described using an plast water effective fractionation factor A a (see Table 1) against 18 16 R0 0/ 0 ratio of C02 in equilibrium with soil 180 on net uptake of CO2. The isotopic exchange flux water between the atmosphere and leaves is thus obtained by Rpdb 180/160 ratio of CO2 derived from the carbonate multiplying Aa by net flux of CO2 into the leaves (basi­ standard Pee-Dee Belemnite [see Friedman and cally equal to gross primary production, GPP). The fac­ O'Neil, 1977] tor Aa is not a true fractionation factor because it de­ 6a (Ra-RPDB)/RPDB pends on the isotopic composition of atmospheric CO2. 6c (Rc—Rpdb)/Rpdb Aa is nevertheless useful because it can be measured 63 (R«—Rpdb)/Rpdb in controlled experiments as well as modeled over the 6r 68 + e80u surface of the earth [Farquhar et al, 1993]. Fin Gross flux of CO2 into stomata The latitudinal distribution of Aa as estimated by Fout Gross flux of CO2 out of stomata Farquhar et al [1993], is shown in Figure 2. Also shown R Flux of CO2 out of soil from root and soil respiration is the latitudinal variation of C02 in equilibrium with surface seawater (6°), the isotopic composition of CO2 ttsto Fractionation factor of diffusion through stomata (same both directions) returned to the atmosphere through soils (6r), the sum 1S or8oii Fractionation factor for diffusion out of soil 6r + AA, and the annual mean surface values of S 0 —5 er Csto Qfsto ~ 1 [ P Farquhar et al., 1993] of atmospheric CO2.