Ecosystem Responses Of Pine And Sweetgum Forests To Elevated Co2

Although there is a rich understanding of the response of potted plants and small trees to elevated CO2, until recently experiments had not been conducted at an appropriate spatial and temporal scale to examine the effect of elevated CO2 on ecosystem processes regulating the C cycle. With the development of FACE technology (Hendrey et al., 1999; McLeod and Long, 1999; Miglietta et al., 2001; Okada et al., 2001), it became possible to elevate atmospheric CO2 in large plots in intact ecosystems without altering other microclimatic variables and without restricting the movement of animals, including important herbivores. Initially employed in agricultural systems (Hendrey and Kimball, 1994; Kimball et al., 2002), approximately 24 FACE experiments currently are underway in nonagricultural ecosystems, ranging from deserts and grasslands to large-stature forests (Nowak et al., 2004). Two of the longest running forest experiments, a loblolly pine (Pinus taeda L.) plantation (DeLucia et al., 1999; Naidu and DeLucia, 1999) and a sweetgum (Liquidambar styraciflua L.) plantation (Norby et al., 2001), provide a unique opportunity to examine the responses of contrasting evergreen and deciduous forest ecosystems, respectively, to elevated atmospheric CO2.

Loblolly pine and sweetgum trees are both early succes-sional species of southeastern forests in North America and often compete with one another following agricultural abandonment, with sweetgum favoring moister soils (Keever, 1950). Although these species share similar life history characteristics, the difference in leaf and fine root longevity may directly alter the retention and cycling of C in these different forests, and may further affect the C cycle indirectly by altering the rate of ecosystem nitrogen transformations. Foliage of loblolly pine, an evergreen species, lives for approximately 18 months, whereas sweetgum is a deciduous species, and the leaves live for 6 months or less. Similarly, longevity of loblolly pine fine roots is about 3.4 times longer than that of sweetgum fine roots (Matamala et al., 2003).

In the Duke Forest FACE experiment, 30-m diameter plots in a loblolly pine forest have been exposed to ambient plus 200 pl l-1 CO2 almost continuously since late 1996. This forest, located near Chapel Hill, North Carolina (35° 58' N, 79° 05' W), is on heavily weathered clay-rich Alfisol soils with relatively low nitrogen and phosphorus availability (Schlesinger and Lichter, 2001; Hamilton et al., 2002). Trees were 13 years old when fumigation was initiated. The experimental sweetgum plantation located on the Oak Ridge National Environmental Research Park in Roane County, Tennessee (35° 54' N, 84° 20' W) was established on moderately well-drained, silty-clay-loam soils classified as an Aquatic Hap-ludult; these soils are somewhat richer in nutrients than the pine forest in North Carolina (Norby et al., 2001; George et al., 2003). The sweetgum trees were 10 years old at the initiation of fumigation, slightly younger than the pine forest, and daytime CO2 concentration in the experimental plots has averaged approximately 550 pl l-1 during the growing season since April 1998. These CO2 treatments were chosen for the two experiments because, based on current projections, this CO2 level is anticipated by 2050 (Houghton et al., 2001). Both experiments use the same FACE technology (Hendrey et al., 1999) and include fully instrumented control plots.

Although these experiments employed similar technology to comparably sized forest stands at similar developmental stages, there are important differences between them, and direct comparisons of the results, particularly of the absolute values of various C pools and fluxes, must be treated cautiously. In addition to having a less diverse community of plants in the understory, the sweetgum experiment experiences cooler temperatures and is established on more nutrient rich soils than the pine experiment (Zak et al., 2003). Moreover, estimates of the major ecosystem pools and fluxes of C were made by different investigators who used, in some cases, different scaling approaches and measurements. With these caveats in mind, these contrasting forests provide the most direct and comprehensive comparison of the response of different forests types (evergreen and deciduous) to elevated CO2 currently available.

Exposure to elevated CO2 substantially increased C storage and cycling in these forests (Table 8.1), but the magnitude of stimulation for different components of the carbon budget varied considerably. Gross primary production was stimulated by elevated CO2 to a similar amount (18% to 23%) in the pine and sweetgum plantations. Neither experiment included direct measurement of GPP. In the pine experiment, GPP was estimated as NEP plus ecosystem respiration, which included the sum of the major respiratory C losses from plants and microbes (Re = RSoil + Rwood + Rcanopy + herbivoryaboveground +

dissolved inorganic carbon [DIC]); for sweetgum, it was calculated as NPP plus plant respiration (Ra = Rwood + Rcanopy + Rfine root). Carbon losses by herbivoryaboveground and DIC in the

Table 8.1 Carbon Budgets (g C m-2 year-1) for Loblolly Pine and Sweetgum Forests Under Ambient and Elevated Atmospheric CO2



Table 8.1 Carbon Budgets (g C m-2 year-1) for Loblolly Pine and Sweetgum Forests Under Ambient and Elevated Atmospheric CO2





% A



% A




































Note: GPP = gross primary production, Ra = plant respiration, NPP = net primary production, Rh = heterotroph respiration and NEP = net ecosystem production. Each value represents an average of three (pine) or two (sweetgum) experimental plots. The percent difference between ambient and elevated CO2 plots is indicated by % A. The budget was calculated for plots exposed to elevated CO2 for 2 years for pine and 3 years for sweetgum.

Note: GPP = gross primary production, Ra = plant respiration, NPP = net primary production, Rh = heterotroph respiration and NEP = net ecosystem production. Each value represents an average of three (pine) or two (sweetgum) experimental plots. The percent difference between ambient and elevated CO2 plots is indicated by % A. The budget was calculated for plots exposed to elevated CO2 for 2 years for pine and 3 years for sweetgum.

pine plantation were small and can be ignored (Hamilton et al., 2002). Although a quantitative analysis of the sources of error in these estimates for either forest is not available, it is important to note that a number of simplifying and perhaps imprecise assumptions were employed in scaling the respiratory fluxes measured for individual tissues at a given instant in time to annual values for the entire ecosystem.

Plant respiration (Ra) includes C losses from wood (Rwood; stems, branches, and coarse roots); foliage (Rcanopy), and fine roots (Rflne root). The proportion of GPP lost by Ra appeared greater in the pine (57% to 72%) than in the sweetgum forest (34% to 52%; Table 8.1), but was stimulated by elevated CO2 only in the sweetgum stand. With the exception of foliage, annual respiratory losses were greater from pine wood and fine roots than for sweetgum. Greater tissue specific rates of leaf respiration for sweetgum (Tissue et al., 2002) than for pine (Hamilton et al., 2001) contributed to slightly higher Rcanopy in the former (560 to 570 g C m-2year-1) than in the latter (463 to 492 g C m-2 year-1), even though peak canopy mass was approximately twice as large in the pine (1054 to 1105 g dry matter [DM] m-2) (DeLucia et al., 2002) than in the sweetgum (486 to 553 g DM m-2) (Norby et al., 2003) forest. Respiration from pine stems, branches, and coarse roots (ambient plots: 488 g C m-2year-1; elevated plots: 519 g C m-2 year-1) (Hamilton et al., 2002), although unaffected by CO2 was considerably greater than for sweetgum (ambient plots: 150 g C m-2year-1; elevated plots: 230 g C m-2y-1) (R.J. Norby, 2004, unpublished results, based on Edwards et al.,

2002). As with stems, C losses by Rfine root were higher in the pine forest than the sweetgum forest. Although maintenance respiration per unit root mass was slightly greater in sweet-gum than for pine, the average annual standing biomass of fine roots was two- to three-fold greater in the pine forest (George et al., 2003).

Although it is becoming increasingly evident that short-duration changes in atmospheric CO2 do not affect tissue-specific respiration rates (Hamilton et al., 2001; Davey et al.,

2003), substantial increases in Rwood and Rfine root for trees grown under elevated CO2 contributed to an increase in Ra in the sweetgum forest (Table 8.1). Increased biomass increment and substrate levels under elevated CO2 caused a 23% increase in growth respiration and a 48% increase in maintenance respiration, respectively, for sweetgum stems (Edwards et al., 2002). This stimulation was driven in part by greater wood production under elevated CO2. Given that wood production in the pine forest also was stimulated, it is curious that this forest did not exhibit an increase in Rwood. The answer may be found in the different assumptions about the relative respiration rates of branches vs. boles in these two forests.

Although absolute respiratory losses by fine roots appear lower in the sweetgum forest than the pine forest, elevated CO2 caused a substantial increase in Rfine root only in the former (ambient plots: 245 g C m-2year-1; elevated plots: 455 g C m-2 year-1) (George et al., 2003). Tissue-specific rates of respiration for sweetgum were unaffected, but a 73% increase in the standing mass of fine roots contributed to the large stimulation of Rfine root for this species exposed to elevated CO2.

Greater respiratory losses may have contributed to lower NPP in the pine forest relative to sweetgum, but NPP was substantially increased by elevated CO2 in both forests (Table 8.1). Values of NPP have been calculated somewhat differently at both sites, but these differences have relatively little effect on the absolute values and the magnitude of the treatment effect. For the pine forest, NPP was calculated as the sum of biomass increments (IWood + Ileaf + Icoarse root + Ifine root), plus the major inputs to detritus, litterfall, and fine root turnover (Dlitterfall + Dfine root), plus losses as dissolved organic carbon (DOC) in the soil (Hamilton et al., 2002). For the deciduous sweetgum trees, Ileaf is 0, and root production was calculated directly from minirhizotron analysis rather than from Ifine root plus Dfine root. DOC was not measured. Given these differences and that these forests experience different edaphic factors and climatic regimes, it is not possible to conclude that elevated CO2 caused a greater stimulation of NPP for the pine forest (27%) than for the sweetgum forest (17%). In 2000, when the C budget for sweetgum was calculated, Ra was stimulated by elevated CO2, which provides a plausible explanation for why this forest may have experienced a lesser stimulation of NPP for that year. However, the percent stimulation for sweetgum varied between 16% and 38% depending on the year (Figure 8.3). Calculating long-term averages of the behavior of the more labile C pools will strengthen the direct comparisons of the response of these forests to elevated CO2.

Perhaps more important than the potential differences in the magnitude of the response between these contrasting forest types is the observation that the distribution of the response to elevated CO2 among various C stocks was quite different. Enhanced wood production was the primary factor increasing NPP for the pine forest exposed to elevated CO2 (DeLucia et al., 1999; Hamilton et al., 2002), while the treatment caused a substantial shift in C allocation in sweetgum (Norby et al., 2002). After the first year of exposure to elevated CO2, the stimulation of wood production in sweetgum abated and was replaced by an equivalent increase in fine root production. If these differences are sustained they have important implications for the forest products industry as well as the future role of forests in the global C cycle. A stimulation of

2500 2000 1500 1000 500

2500 2000 1500 1000 500

40 30 20 10

Figure 8.3 Net primary production (NPP; g DM m-2 y-1) for experimental plots in a loblolly pine forest (A) and sweetgum forest (B) exposed to ambient (~370 |l l-1, open bars) and elevated (~570 |l l-1, closed bars) levels of atmospheric CO2. The percent stimulation of NPP (pine, open bars; sweetgum, hatched bars) is illustrated in (C). NPP was calculated as the sum of woody biomass increment and annual litterfall. In the pine forest, the treatment was initiated in August 1996, and some of the 1997 litter was formed before the initiation of the treatment. (Data from D. Moore, E. DeLucia, and R. Norby, unpublished, 2004.)

Figure 8.3 Net primary production (NPP; g DM m-2 y-1) for experimental plots in a loblolly pine forest (A) and sweetgum forest (B) exposed to ambient (~370 |l l-1, open bars) and elevated (~570 |l l-1, closed bars) levels of atmospheric CO2. The percent stimulation of NPP (pine, open bars; sweetgum, hatched bars) is illustrated in (C). NPP was calculated as the sum of woody biomass increment and annual litterfall. In the pine forest, the treatment was initiated in August 1996, and some of the 1997 litter was formed before the initiation of the treatment. (Data from D. Moore, E. DeLucia, and R. Norby, unpublished, 2004.)

harvestable wood production, particularly in young pine stands, will be beneficial to the forestry industry (Groninger et al., 1999), and provided that this wood is used in durable products, will contribute to a net removal of C from the atmosphere. Allocation of extra C to highly labile fine roots in sweetgum, however, may contribute far less to C sequestration in biomass, as the mean residence time of C in sweetgum fine roots is just 1.2 years (Matamala et al., 2003). Although the potential for C sequestration in biomass is less, more C is cycled into the soil in the sweetgum forest, where there is a potential for some of it to be sequestered in soil organic matter.

In both forests, the increases in NPP with elevated CO2 were driven by greater rates of biomass accumulation associated with a stimulation of photosynthesis rather than increases in the capacity of the forest canopy to capture light energy. The canopies of both forests at the time these C budgets were calculated were at their maxima, with leaf area indices (LAI) of ~4 and ~6 for the pine and sweetgum forest, respectively (DeLucia et al., 2002; Norby et al., 2003). The stimulation of biomass increment without corresponding increases in LAI and light absorption resulted in 23% to 27% stimulation in radiation-use efficiency (e), defined as biomass increment per unit absorbed photosynthetically active radiation. Values of e for the sweetgum forest (2001 ambient plot: 2.01 g MJ-1 and elevated plot: 2.48 g MJ-1) (Norby et al., 2003) were considerably greater than for the pine forest (ambient plot: 0.49 g MJ-1; elevated plot: 0.62 g MJ-1) (DeLucia et al., 2002). Most of the difference in the absolute magnitude of e between these forests is likely to stem from the year-round light absorption in pine without corresponding growth during the winter. In fact, the ratio of NPP/LAI, a proxy for e, is remarkably similar between forests (pine: 176; sweetgum: 170). Current evidence suggests that LAI and light absorption of forests is not likely to be affected by increasing CO2.

Calculation of microbial respiration from the soil (Rh) continues to be problematic, as it requires differentiating C derived from plant roots from C derived from soil microorganisms (Kelt-ing et al., 1998; Edwards and Norby, 1999), yet quantifying this variable is important for estimating NEP from NPP. The pine and sweetgum experiments used different approaches to solve this problem. In the pine experiment Rh was estimated as the difference between Rsoil and Rfine root; where Rsoil was measured as CO2 efflux from the soil surface (Andrews and Schlesinger, 2001), and Rgne root was calculated as the product of standing root biomass and temperature-adjusted respiration rates measured on unearthed but attached roots (Hamilton et al., 2002; George et al., 2003). For the sweetgum forest, Rh was calculated as the product of Rsoil and the ratio of fine root-to-microbial respiration (Rfine root/Rh), where the ratio Rfine root/Rh was based on an analysis of the isotopic composition of C evolved from the soil, as in Andrews et al. (1999). In sharp contrast to Ra, estimates of Rh revealed a strong stimulation by elevated CO2 in the pine forest (166%) compared to the sweetgum forest (9%) (Table 8.1).

A number of factors may have contributed to the differential responsiveness of Rh to elevated CO2 in these forests, including broad differences in the composition of the soil microbial communities. Pine roots, for example, are associated with ectomycorrhizal fungi, while sweetgum roots are associated with vesicular-arbuscular mycorrhizal fungi. In addition, elevated CO2 disproportionately stimulated litter inputs of C to the soil in the pine relative to the sweetgum forest, thereby providing more substrate for soil microbial populations. Leaf litter represents a highly labile C source, and the amount of litter was ~19% greater in the elevated CO2 plots in the pine forest (Finzi et al., 2001), but only ~10% greater in the elevated CO2 plots in the sweetgum forest (Norby et al., 2003). The nutrient contents of pine and hardwood leaf litter in the pine forest were unaffected by growth under elevated CO2 (Finzi et al., 2001); microbial populations in this forest should therefore respond solely to the increased input of litter C. Nitrogen concentration is significantly lower in the CO2-enriched sweetgum litter, but since the litter decomposes so quickly, potential effects of litter quality on decomposition are minimal (Johnson et al., 2004).

NEP was stimulated by elevated CO2 and the absolute values were comparable between these forests (Table 8.1). For the pine experiment, NEP was calculated as the sum of biomass increments plus the increase in forest floor biomass (Iwood

+ Ileaf + Icoarse root + Ifine root + Iforest floorX in the sweetgum fore^

NEP was calculated as NPP - Rh. That NEP was calculated independently from the respiratory fluxes in the pine forests revealed an interesting and potentially important inconsistency. While this estimate of NEP is consistent with the value calculated as NPP - Rh for the ambient plots, there is a large discrepancy for the elevated CO2 plots, where NEP calculated by subtraction is only ~54% of the value presented in Table 8.1. This discrepancy suggests that the estimate of Rfine root for this forest is too small, or the value of Rh is too large or some combination of the both. Andrews et al. (1999) estimated that the root contribution to Rsoil was 55% under elevated CO2, similar to the 48% in this analysis, suggesting that many small errors may have contributed to this discrepancy. A similar inability to close the C budget for this pine forest under elevated CO2 was recently reported by Schäfer et al. (2003).

Ignoring human-induced changes in land cover, NEP represents C sequestration in ecosystems (International Geo-sphere-Biosphere Programme, 1998). There is great uncertainty about the potential for forest ecosystems to abate the accumulation of anthropogenic C in the atmosphere and the contribution of the CO2-fertilization effect to the observed residual terrestrial C "sink" of ~2.8 Gt year-1. Recent evidence suggests that reforestation and aforestation in eastern North America and Western Europe contribute substantially to this sink (Fan et al., 1998; Pacala et al., 2001; Janssens et al., 2003). How much of this sink is derived from changes in land use relative to stimulations in tree growth caused by elevated CO2, nitrogen deposition and climate remains controversial. Schimel et al. (2000) estimate that as much as one third of additional C stored in forest ecosystems in North America is derived from a combined stimulation of tree growth by CO2 and climate, whereas Caspersen et al. (2000) estimate that approximately 2% but with an upper limit of 7% of the observed increase in aboveground net ecosystem production was caused by a CO2-stimulation of growth. Although their approach has been criticized for not being sufficiently robust to estimate small changes in growth (Joos et al., 2002), this upper limit is consistent with experimental data.

Based on the observed stimulation of NEP in these forests and assuming that the response of NEP to CO2 is linear, the ~55 pl l-1 increase in CO2 between 1930 and 1995, the approximate interval examined by Caspersen et al. (2000), should have contributed to an 8% to 12% stimulation in C sequestration. Although young forests have considerable capacity to respond to increases in atmospheric CO2, the magnitude of the responses observed for these forests suggests that the effect of changes in land use on C sequestration are greater than the effect of a CO2-induced growth stimulation. Detecting a response to CO2 that is independent of other environmental influences, stand developmental history, and regional-scale land-use patterns remains a problem.

The Duke and the Oak Ridge FACE experiments provide novel insights into the response of forest ecosystems to an increase in atmospheric CO2, but the picture they paint is incomplete. Both experiments exposed trees to a step change in CO2 — one day the experimental plots experienced ambient CO2 and the next day and from then on it was elevated to the level expected in the year 2050. Extrapolations from perturbation experiments such as these are difficult because ecosystem C sequestration rates are projected to respond differently to gradual vs. step increases in atmospheric CO2 (Luo et al., 2003). Respiration is generally proportional to the sizes of various C pools, and increases in pool sizes are cumulative. The difference between a step increase in GPP and a gradual increase in respiration translates to a transient response in C sequestration rate (Luo et al., 2003). Hence, we cannot assume that the effect of CO2 enrichment on stimulation of NEP in these experiments will persist. By compiling several data sets including growth measurements of trees growing next to natural CO2 springs, Idso (1999) concluded that the growth stimulation caused by elevated CO2 attenuates strongly with time. A second but no less important limitation of these experiments is that trees are exposed to elevated CO2, but without the intimately related increase in air temperature that is expected, leaving the question unresolved of how elevated CO2 and temperature interact to affect C cycling. The recent construction of a forest nitrogen budget for the Duke loblolly pine experiment and an analysis of interannual variation in the growth response to elevated CO2 for this forest provide tentative answers to these questions.

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