Carbon is transferred through and stored in ecosystems by a myriad of physiological, ecological, and geochemical processes (Schlesinger, 1997; Clark et al., 2001) that may respond independently to the different facets of global change. Microbial respiration in the soil, for example, is extraordinarily sensitive to temperature, whereas photosynthesis responds strongly to changes in both atmospheric CO2 and temperature. Predicting the effects of changing climatic conditions and atmospheric chemistry on the C cycle requires a clear understanding of these different processes. Broadly defined, C cycles comprise pools and fluxes, where a pool is a C reservoir lasting 1 year or longer (Hamilton et al., 2002), and fluxes represent the rates of C transfer from one pool to another. C pools typically are expressed per unit land area; fluxes are expressed per unit land area per annum. Although the major processes (fluxes) and pools in ecosystem C cycles were identified over 30 years ago (Whittaker, 1975), quantification of many of these processes remains clouded with uncertainty, and few studies have attempted to "close" the C budget for individual forest stands. The following discussion presents the currently held definitions for the major process regulating the flow of C through forest ecosystems and highlights a few of the most important uncertainties in their quantification.
Carbon enters ecosystems from the atmosphere by net photosynthesis, and is expressed as gross primary production (GPP) (Figure 8.1). Here photosynthesis is defined as the net reduction of CO2 by plant canopies to sugars and structural materials. This net value represents C fixed by the primary carboxylating enzyme in chloroplasts, rubisco (rubisco: ribu-lose bisphosphate carboxylase-oxygenase [EC 188.8.131.52]), minus the amount immediately returned to the atmosphere by photorespiration, but does not include oxidative respiration in mitochondria. GPP cannot be directly measured because of the need to separate C uptake by photosynthesis and losses by mitochondrial respiration. At the stand or ecosystem level,
GPP typically is estimated by scaling appropriate leaf-specific measurements in space and time (Wofsy et al., 1993), by process-based models (Aber et al., 1996; Luo et al., 2001), or calculated from stand-level estimates of transpiration (Schäfer et al., 2003). Alternatively, the sum of all subordinate C increments and losses can be used to calculate the rate of GPP necessary to meet these demands (Ryan et al., 1996; Hamilton et al., 2002).
Particularly in monospecific stands where obtaining representative physiological parameters and a physical description of the canopy are relatively straightforward, process-based models provide an effective means of calculating GPP. In many models, the strength of this approach stems from the rigorous and mature theory relating the biochemistry of carbon fixation to leaf biochemical properties and environmental conditions (von Caemmerer, 2000).
Once CO2 becomes chemically reduced by photosynthesis, carbohydrates are expended to meet metabolic needs of plants and the corresponding rates of autotrophic respiration (Ra) result in a substantial return of C back to the atmosphere, globally amounting to ~64 Gt yr-1 (Figure 8.1). Carbohydrates consumed in oxidative respiration by mitochondria are used to support the maintenance and construction of plant tissues in roots, stems, and foliage. Assumed to be 50% of GPP (Waring et al., 1998), Ra can exceed 70% of GPP in some forests (Hamilton et al., 2002) and varies with forest age (Makela and Valentine, 2001). Because of the shear magnitude of Ra and its strong sensitivity to temperature, it is an important process defining the capacity of forests to store atmospheric C (Valentini et al., 2000).
The calculations of respiratory fluxes at the ecosystem level are made by scaling tissue specific rates, usually as a function of tissue nitrogen content and temperature (Ryan, 1995; Ryan et al., 1996; Hamilton et al., 2002; Meir and Grace, 2002), or measured directly at the stand level by micromete-orological methods (Baldocchi et al., 1988; Baldocchi, 2003). Unfortunately, the current understanding of environmental and physiological regulation of Ra is far from complete.
In contrast to photosynthesis, there is no theory for predicting variation in respiration rates for individual tissues. Respiration used to maintain cellular integrity, build ion gradients, and transport materials is highly sensitive to temperature, and this sensitivity results in a strong relationship between short-term variation in temperature and the rates of CO2 evolution by plant tissues (Atkin and Tjoelker, 2003). The temperature dependence of Ra provides a convenient tool for extrapolating tissue-specific rates to the stand level. However, the rate of oxidative respiration also varies with the supply of carbohydrates, resulting in a linkage to the rate of photosynthesis and to the utilization of carbohydrates by sink tissues (Dewar et al., 1999; Atkin and Tjoelker, 2003). Under this form of control, respiration rates should vary with photosynthesis, as is implied by the observed correlation between Ra and GPP (Waring et al., 1998). The absence of a clear understanding of when seasonally and when during ecosystem development that Ra is under temperature or substrate control is a major impediment to estimating its response to current and future conditions.
The origin of respired CO2 is not always clear, which contributes additional uncertainty to our estimates of ecosystem Ra. The fraction of soil respiration derived from plant roots vs. soil microbes (Andrews et al., 1999), the capacity of C to move in solution in the transpiration stream through trees (Teskey and McGuire, 2002), and "contaminate" estimates of bole respiration, and the activity of mitochondrial respiration during photosynthesis (Loreto et al., 2001; Wang et al., 2001) are just a few of the uncertainties that undermine quantitative estimates of Ra. An improved understanding of the origins and regulation of plant respiration under field conditions will greatly enhance the accuracy of forest carbon budgets.
Net primary production (NPP) is the difference between GPP and Ra; in addition to providing energy in the form of reduced C compounds for nonphotosynthetic organisms, NPP contributes to the accumulation of C in ecosystems. In contrast to GPP and Ra, the annual increment of woody tissue, a major component of NPP in forest ecosystems, can be estimated directly from measurements of diameter growth and allomet-ric relationships. However, a number of processes, some small and some large, often are not included and their absence may contribute to substantial underestimates of NPP (Clark et al., 2001). NPP includes the annual production of foliage as well as coarse and fine roots. Estimating fine root production and turnover is inherently difficult (Nadelhoffer and Raich, 1992; Publicover and Vogt, 1993; Hertel and Leuschner, 2002), which is compounded by high spatial variability within forests. The contribution of fine root production to NPP range from 33% to 67% (Jackson et al., 1997; Grier et al., 1981; Santantonio and Grace, 1987), and recent evidence that root longevities may have been substantially underestimated (Matamala et al., 2003) will likely alter these previous estimates. The production of short-lived materials (less than 1 year), including losses of dissolved organic carbon, and herbivory and volatilized organic compounds should be included (Clark et al., 2001), although with the exception of leaf litter, these other elements tend to be relatively small proportion of NPP. Herbivory, fine root mortality, and losses of volatile and nonvolatile organic compounds contributed to less than 10% of NPP in a rapidly growing loblolly pine plantation (Hamilton et al., 2002).
Globally, heterotrophic respiration (Rh) returns approximately 56 Gt C to the atmosphere each year; similar to the amount from Ra and almost ten times more than the amount of C injected into the atmosphere annually from the combustion of fossil fuels (Figure 8.1). Most of this flux is derived from rhizosphere and soil organisms including bacteria, fungi, and soil invertebrates. Estimates of Rh suffer from many of the same scaling issues as Ra, and present an additional formidable challenge — separating Rh from root-derived Ra. Carbon dioxide evolved from soils is derived from a combination of autotrophic respiration from plant roots and soil microorganisms, and assigning this C to the proper source is critical for determining NPP and NEP. Mycorrhizal fungi and bacteria living in the sphere of influence of fine roots, the rhizo-sphere, raise an additional problem. Should they be considered part of the root or part of the soil C budget? Wiant (1967) argued that root respiration should include all processes oxidizing plant-derived organic compounds in and on the surface of fine roots, including mycorrhizal fungi and microorganisms oxidizing root exudates.
Hanson et al. (2000) identified three general approaches to quantify the contribution of Ra and Rh to soil CO2 efflux. The first approach, "component integration," involves physically isolating and measuring the individual fluxes of different components of the plant-soil system and then adding them up. Hamilton et al. (2002) and George et al. (2003) used a variation of this approach to quantify the belowground C budget for a pine forest and a sweetgum forest exposed to elevated CO2; Rh was calculated as the difference between total soil CO2 efflux and the respiration rate of unearthed fine roots. The potential effects of disturbing the plant-soil system are the primary limitations of this approach. The second category includes various methods of "excluding roots," by inserting barriers or digging trenches in the soil, physically removing roots, or measuring soil CO2 fluxes from soil under large canopy gaps where the influence of plant roots presumably is minimal. Disturbance effects and large increases in CO2 efflux derived from rapid decomposition of newly severed roots are potential limitations of these methods. The third approach includes various methods of "isotope labeling," where intrinsic variation in soil and root C isotopic composition or the introduction of a label is used to identify the source of respired CO2. Andrews et al. (1999) used the sudden exposure of an intact pine forest to 13C-depleted air to determine that roots contributed 55% of total soil respiration at the surface late in the growing season.
Estimates of the contribution of Ra derived from roots to total soil CO2 efflux vary considerably. In a literature survey, Hanson et al. (2000) reported that the median value for the contribution of Ra to total soil CO2 efflux was 50% to 60%. However, ~31% of the studies in this survey reported a percent contribution of fine roots to soil CO2 efflux of at least 60%, and ~20% of the studies reported a proportional root contribution of at least 40%. A recent study of a rapidly growing pine plantation indicated that Rh was ~22% of total soil CO2
efflux, but increased sharply in plots exposed to elevated levels of atmospheric CO2 (Hamilton et al., 2002).
Net ecosystem production (NEP) is of great importance to our understanding of the transfers of C between the atmosphere and terrestrial ecosystems as it represents the net accumulation of C in ecosystems, and thus provides a measure of C sequestration. As defined by Woodwell and Whittaker (1968), NEP is the difference between NPP and heterotrophic respiration (Rh). This definition is incomplete in that it does not include a number of nonrespiratory fluxes, such as C losses as volatile organic carbon and methane (Randerson et al., 2002). While the absolute magnitude of these nonrespiratory losses often is small (e.g., Hamilton et al., 2002), the impact of these molecules can be quite large. For example, the volatile organic compound isoprene is a precursor to tro-pospheric ozone, a potent oxidant with enormous potential to reduce ecosystem productivity. A more inclusive definition of NEP, therefore, is simply the change in total C stocks in a given ecosystem over time (Randerson et al., 2002). Net biome production (NBP) (Schulze and Heimann, 1998) is functionally equivalent to NEP, but applies to regional C increments and losses from fire, harvest, and other episodic disturbances. Although mathematically simple, quantifying NEP represents a formidable challenge.
Setting aside modeling approaches (Aber et al., 1996; Kicklighter et al., 1999; Waring and McDowell, 2002) and inversion methods based on static gas sampling of the atmosphere (Pacala et al., 2001), estimation of net C storage in ecosystems takes one of three approaches: (1) direct measurement of C fluxes, either by chamber or micrometeorological methods; (2) physiological scaling in combination with bio-metric measurements; or (3) direct measurement of C stocks over time, either within a site or along a chronosequence. The chamber and micrometeorological methods require a continuous record of C fluxes for a given ecosystem over an entire year that is either measured or backfilled with a model. The annual integral of net ecosystem exchange by these methods is equivalent to NEP.
Chamber-based measurements are restricted to low-stature communities (e.g., Drake et al., 1996; Shaver et al., 1998; Dore et al., 2003; Obrist et al., 2003) and require intermittent sampling, while the eddy flux method provides a continuous record of CO2 fluxes over relatively large land areas (Baldocchi et al., 1988; Curtis et al., 2002; Baldocchi, 2003). For forest ecosystems, this latter micrometeorological approach is not amenable to comparative studies involving relatively small plots. In free-air CO2 enrichment (FACE) experiments, for example, where the plot size exposed to ambient or elevated levels of atmospheric CO2 is less than 1/10 ha (DeLucia et al., 1999; Norby et al., 2002), the scaling of physiological fluxes combined with biometric estimates of standing biomass (O'Connell et al., 2003) or direct measurement of changes in C stocks (Boone et al., 1988; Lichter, 1998) are more appropriate for estimating NEP. In accounting for changes in C stocks through time, particular attention is paid to changes in live and dead vegetation, the major components of NEP, with smaller changes in forest floor and soil C (Boone et al., 1988; Hamilton et al., 2002). Approaches to estimating NEP from physiological scaling suffer from the same uncertainties employed in estimating Ra and Rh discussed above. Changes in most C stocks can readily be measured on annual or greater time steps, but often it is difficult to detect change in soil C pools over relatively short periods.
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