As noted in our Carbon Sequestration Commentary of 18 Sep 2002, atmospheric CO2 enrichment stimulates photosynthesis in nearly all plants, typically producing more non-structural carbohydrates, which can be used to manufacture more carbon-based secondary compounds (CBSCs) or phenolics. This observation is important because phenolics tend to inhibit the decomposition of the organic matter in which they are found (Freeman et al., 2001). Hence, if elevated levels of atmospheric CO2 lead to the production of more of these decay-resistant substances, one would expect the ongoing rise in the air's CO2 content to lead to the enhanced sequestration of plant-litter-derived carbon in the world's soils, producing a negative feedback phenomenon that would tend to slow the rate of rise of the air's CO2 content and thereby moderate CO2-induced global warming. So what do experiments reveal about this hypothesis?
For a long time the picture was rather muddled. Many studies reported the expected increases in CBSC concentrations with experimentally-created increases in the air's CO2 content. Others, however, could find no significant plant phenolic content changes; while a few even detected CO2-induced decreases in CBSC concentrations. Although chaos thus reigned in this area for some time, Penuelas et al. (1997) finally brought order to the issue when they identified the key role played by soil nitrogen.
In analyzing the results of several different studies, Penuelas et al. noticed that when soil nitrogen supply was less than adequate, some of the CBSC responses to a doubling of the air's CO2 content were negative, i.e., a portion of the studies indicated that plant CBSC concentrations actually declined as the air's CO2 content rose. When soil nutrient supply was more than adequate, however, the responses were almost all positive, with plant CBSC concentrations rising in response to a doubling of the air's CO2 concentration. In addition, when the CO2 content of the air was tripled, all CBSC responses, under both low and high soil nitrogen conditions, were positive.
The solution to the puzzle was thus fairly simple. With a tripling of the air's CO2 content, nearly all plants exhibited increases in CBSC production; but with only a doubling of the atmospheric CO2 concentration, adequate nitrogen was needed to ensure a positive CBSC response.
What makes these observations especially exciting is that atmospheric CO2 enrichment, in addition to enhancing plant growth, typically stimulates nitrogen fixation in both woody (Olesniewicz and Thomas, 1999) and non-woody (Niklaus et al., 1998; Dakora and Drake, 2000) legumes. Hence, as the air's CO2 content continues to rise, earth's nitrogen-fixing plants should become ever more proficient in this important enterprise. In addition, some of the extra nitrogen thus introduced into earth's ecosystems will likely be shared with non-nitrogen-fixing plants. Also, since the microorganisms responsible for nitrogen fixation are found in nearly all natural ecosystems (Gifford, 1992), and since atmospheric CO2 enrichment can directly stimulate the nitrogen-fixing activities of these microbes (Lowe and Evans, 1962), it can be appreciated that the ongoing rise in the air's CO2 content will likely provide more nitrogen for the production of more CBSCs in all of earth's plants. And with ever-increasing concentrations of decay-resistant materials being found throughout plant tissues, the plant-derived organic matter that is incorporated into soils should remain there for ever longer periods of time.
On the other hand, in a meta-analysis of the effects of atmospheric CO2 enrichment on leaf-litter chemistry and decomposition rate that was based on a total of 67 experimental observations, Norby et al. (2001) found that elevated atmospheric CO2 concentrations - mostly between 600 and 700 ppm - reduced leaf-litter nitrogen concentration by about 7%. But in experiments where plants were grown under as close to natural conditions as possible, such as in open-top chambers, FACE plots, or in the proximity of CO2-emitting springs, there were no significant effects of elevated CO2 on leaf-litter nitrogen content.
In addition, based on a total of 46 experimental observations, Norby et al. determined that elevated atmospheric CO2 concentrations increased leaf-litter lignin concentrations by an average of 6.5%. However, these increases in lignin content occurred only in woody, but not herbaceous, species. And again, the lignin concentrations of leaf litter were not affected by elevated CO2 when plants were grown in open-top chambers, FACE plots, or in the proximity of CO2-emitting springs.
Finally, in an analysis of a total of 101 observations, Norby et al. found that elevated CO2 had no consistent effect on leaf-litter decomposition rate in any type of experimental setting. Hence, as the air's CO2 content continues to rise, it will likely have little to no impact on leaf-litter chemistry and rates of leaf-litter decomposition. Since there will be more leaf litter produced in a high-CO2 world of the future, however, that fact alone will ensure that more carbon is sequestered in the world's soils for longer periods of time, as also noted in our Carbon Sequestration Commentary of 28 Nov 2001.
It must additionally be noted, however, as stated by Agren and Bosatta (2002), that "global warming has long been assumed to lead to an increase in soil respiration and, hence, decreasing soil carbon stores." Indeed, this dictum was accepted as gospel for many years, for a number of laboratory experiments seemed to suggest that nature would not allow more carbon to be sequestered in the soils of a warming world. As one non-laboratory experiment after another has recently demonstrated, however, such is not the case; and theory has been forced to change to accommodate reality.
The old-school view of things began to unravel in 1999, when two important studies presented evidence refuting the long-standing orthodoxy. Abandoning the laboratory for the world of nature, Fitter et al. (1999) heated natural grass ecosystems by 3°C and found that the temperature increase had "no direct effect on the soil carbon store." Even more astounding, Liski et al. (1999) showed that carbon storage in the soils of both high- and low-productivity boreal forests in Finland actually increased with rising temperatures along a natural temperature gradient.
The following year saw more of the same. Johnson et al. (2000) warmed natural Arctic tundra ecosystems by nearly 6°C for eight full years and still found no significant effect of that major temperature increase on ecosystem respiration. Likewise, Giardina and Ryan (2000) analyzed organic carbon decomposition data derived from the forest soils of 82 different sites on five continents, reporting the amazing fact that "despite a 20°C gradient in mean annual temperature, soil carbon mass loss ... was insensitive to temperature."
What was theory to do? It had to change. What is more, it had to change fast. And it did. The very next year, Thornley and Cannell (2001) ventured forth gingerly with what they called "an hypothesis" concerning the matter. Specifically, they proposed the idea that warming may increase the rate of certain physico-chemical processes that transfer organic carbon from less-stable to more-stable soil organic matter pools, thereby enabling the better-protected organic matter to avoid, or more strongly resist, decomposition. Then, they developed a dynamic soil model in which they demonstrated that if their thinking was correct, long-term soil carbon storage would appear to be insensitive to a rise in temperature, even if the respiration rates of all soil carbon pools rose in response to warming, as they indeed do.
The paper of Agren and Bosatta is an independent parallel development of much the same concept, although they describe the core idea in somewhat different terms, and they upgrade the concept from what Thornley and Cannell call an "hypothesis" to what they refer to as the continuous-quality "theory." Quality, in this context, refers to the degradability of soil organic matter; and continuous quality suggests there is a wide-ranging continuous spectrum of soil organic carbon "mini-pools" that possess differing degrees of resistance to decomposition.
The continuous quality theory thus states that soils from naturally higher temperature regimes will have soil organic matter "continuous quality" distributions that contain relatively more organic matter in carbon pools that are more resistant to degradation and are consequently characterized by lower rates of decomposition, which has been observed experimentally to be the case by Grisi et al. (1998). In addition, it states that this shift in the distribution of soil organic matter qualities, i.e., the higher-temperature-induced creation of more of the more-difficult-to-decompose organic matter, will counteract the decomposition-promoting influence of the higher temperatures, so that the overall decomposition rate of the totality of organic matter in a higher-temperature soil is either unaffected or actually reduced.
Once again, therefore, it would appear that the ongoing rise in the air's CO2 content, as well as any degree of warming that might possibly accompany it, will not materially alter the rate of decomposition of the world's soil organic matter. Hence, the rate at which carbon is sequestered in the world's soils should continue to increase, as joint function of the rate at which the productivity of earth's plants is increased by the aerial fertilization effect of the rising atmospheric CO2 concentration and the rate of expansion of the planet's vegetation into drier regions of the globe that is made possible by the concomitant CO2-induced increase in vegetative water use efficiency.
References
Agren, G.I. and Bosatta, E. 2002. Reconciling differences in predictions of temperature response of soil organic matter. Soil Biology & Biochemistry 34: 129-132.
Dakora, F.D. and Drake, B.G. 2000. Elevated CO2 stimulates associative N2 fixation in a C3 plant of the Chesapeake Bay wetland. Plant, Cell and Environment 23: 943-953.
Fitter, A.H., Self, G.K., Brown, T.K., Bogie, D.S., Graves, J.D., Benham, D. and Ineson, P. 1999. Root production and turnover in an upland grassland subjected to artificial soil warming respond to radiation flux and nutrients, not temperature. Oecologia 120: 575-581.
Freeman, C., Ostle, N. and Kang, H. 2001. An enzymic 'latch' on a global carbon store. Nature 409: 149.
Giardina, C.P. and Ryan, M.G. 2000. Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404: 858-861.
Gifford, R.M. 1992. Interaction of carbon dioxide with growth-limiting environmental factors in vegetative productivity: Implications for the global carbon cycle. Advances in Bioclimatology 1: 24-58.
Grisi, B., Grace, C., Brookes, P.C., Benedetti, A. and Dell'abate, M.T. 1998. Temperature effects on organic matter and microbial biomass dynamics in temperate and tropical soils. Soil Biology & Biochemistry 30: 1309-1315.
Johnson, L.C., Shaver, G.R., Cades, D.H., Rastetter, E., Nadelhoffer, K., Giblin, A., Laundre, J. and Stanley, A. 2000. Plant carbon-nutrient interactions control CO2 exchange in Alaskan wet sedge tundra ecosystems. Ecology 81: 453-469.
Liski, J., Ilvesniemi, H., Makela, A. and Westman, C.J. 1999. CO2 emissions from soil in response to climatic warming are overestimated - The decomposition of old soil organic matter is tolerant of temperature. Ambio 28: 171-174.
Lowe, R.H. and Evans, H.J. 1962. Carbon dioxide requirement for growth of legume nodule bacteria. Soil Science 94: 351-356.
Niklaus, P.A., Leadley, P.W., Stocklin, J. and Korner, C. 1998. Nutrient relations in calcareous grassland under elevated CO2. Oecologia 116: 67-75.
Norby, R.J., Cotrufo, M.F., Ineson, P., O'Neill, E.G. and Canadell, J.G. 2001. Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia 127: 153-165.
Olesniewicz, K.S. and Thomas, R.B. 1999. Effects of mycorrhizal colonization on biomass production and nitrogen fixation of black locust (Robinia pseudoacacia) seedlings grown under elevated atmospheric carbon dioxide. New Phytologist 142: 133-140.
Penuelas, J., Estiarte, M. and Llusia, J. 1997. Carbon-based secondary compounds at elevated CO2. Photosynthetica 33: 313-316.
Thornley, J.H.M and Cannell, M.G.R. 2001. Soil carbon storage response to temperature: an hypothesis. Annals of Botany 87: 591-598.