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Forested ecosystems are the dominant terrestrial sink for carbon (C) (Schimel et al., 2000; Pacala et al., 2001; Liski et al., 2003). Therefore, determining current and future global C sinks necessitates accurate information on forest responses to increased atmospheric [CO2] and climate change. Of particular interest is whether forest growth and C storage will increase under future conditions, possibly mitigating some of the human-induced rise in [CO2]. Presently, there is growing recognition that plant growth responses to increased [CO2] will not be as large as initially expected, and enhancements will not be uniform across the landscape, as a result of the uneven distribution of other growth resources, such as water and nutrients (e.g. Oren et al., 2001; Gill et al., 2002; Nowak et al., 2004; Körner, 2006). However, there is inadequate quantification of how elevated [CO2] may interact with the spatial and temporal heterogeneity of other growth resources, making it difficult to include such interactions in models that project future forest responses.
Net primary productivity (NPP) is generally expected to increase with increasing concentrations of atmospheric CO2. A recent synthesis of NPP across four temperate closed-canopy forest free-air CO2 enrichment (FACE) sites found a surprisingly consistent enhancement, averaging 23% (Norby et al., 2005). However, this uniform response of the average NPP did not take into account the considerable variability that occurred within each site (Norby et al., 2005), possibly caused by variation in resource availability (e.g. Finzi et al., 2002). Previous studies at the Duke FACE site demonstrated that the [CO2]-induced enhancement of NPP was strongly related to nitrogen (N) availability through the positive effect of N availability on leaf area (McCarthy et al., 2006a). Efforts to characterize how interactions between [CO2] and N availability affect NPP during the second rotation of Populus species in Italy (POP-EUROFACE) failed because previous usage as agricultural land rendered the site N unlimited (Liberloo et al., 2006). Overall, few studies have examined C dynamics under elevated [CO2] within the context of stand development, or have explicitly taken advantage of natural variability in climate and resource availability to increase the relevance of FACE research for predicting future forest function (Osmond et al., 2004).
Determining the effects of elevated [CO2] on forest ecosystem function and C storage requires not only knowledge of the degree to which elevated [CO2] will enhance tree biomass, but also where the additional C will be allocated. Carbon partitioning (i.e. the fraction of total production used by a given component; Litton et al., 2007) affects C storage in two ways: first, partitioning to leaves or fine roots determines the ability of plants to capture additional resources; and, second, different plant parts turn over at different rates, so that partitioning to slow turnover parts (e.g. stems), or to parts that contribute to very slow-turning pools (e.g. soil C) would increase the residence time and C storage. The traditional view of allocation is that plants allocate their resources (C and nutrients) in such a way as to optimize their gain of further resources (including water), in response to their growth environment (e.g. Thornley, 1972; Dewar, 1993; McConnaughay & Coleman, 1999). According to these principles, an optimal allocation strategy would suggest that plants growing under elevated concentrations of atmospheric CO2 should allocate proportionally more C to root formation, in order to exploit soil resources more fully (i.e. to increase water and nutrient uptake). Furthermore, the magnitude of this response should be driven by soil resource availability, with more nutrient or water-limited systems showing a greater increase in fine root allocation (e.g. Palmroth et al., 2006; Litton et al., 2007).
Free-air CO2 enrichment sites allow empirical testing of these theoretical principles, by exposing an ecosystem to a new set of conditions and observing whether the theoretical behavior (or optimum) is achieved (Dewar et al., 2009). Thus far, experimental results from the FACE sites at both Duke and the Oak Ridge National Laboratory (ORNL) have been used in such tests. At the Duke FACE site a majority of the extra NPP was allocated to wood production (DeLucia et al., 2005). Similarly, in the sweetgum (Liquidambar styraciflua L.) plantation at the ORNL FACE site (stand age 10 yr at the initiation of [CO2] enrichment), a majority of the extra NPP was partitioned to wood production during the first year of [CO2] enhancement; however, after 3 yr, 75% of the [CO2]-induced enhancement was partitioned to short-lived fine roots and foliage (Norby et al., 2002, 2004). The disparity in allocation to fine roots occurred even though both Duke and ORNL FACE sites are considered to be N-limited sites (Finzi et al., 2007). However, a recent application of a growth-optimization model correctly predicted these differing fine root allocation patterns at both sites based on changes in ‘apparent’ available soil N and differing root longevity (3 vs 0.53 yr; Franklin et al., 2009). A recent synthesis of the largely accurate performances of several optimization models also suggests that models of this type may be useful for predicting global change effects on allocation patterns (Dewar et al., 2009). However, additional data are needed to validate these models.
Studies of trees or ecosystems under elevated [CO2] have primarily focused on average responses, seldom proceeding further to assess how responses to changes in [CO2] may depend on other growth resources, such as water and N (c.f. Finzi et al., 2002). Furthermore, most studies on the effect of elevated [CO2] on trees and forests are too brief to permit separating treatment effects on partitioning via the effect on the rate of development from the direct effects at comparable developmental stages (Körner, 2006). Our study, performed at the Duke FACE site, combines the results of 10 yr of studies on plant C pools and fluxes in order to assess the long-term effects of elevated [CO2] on stand development, as reflected in C production and partitioning. These data were collected during a time period with a broad range of climatic conditions and from a site with a variation of nearly 2.5-fold in natural N availability, allowing us to quantify how much productivity and partitioning are affected by water and N availability, and how the [CO2]-induced response is affected by these two factors. The objective of this study was to examine the long-term effects of elevated [CO2] on stand C dynamics, focusing on the following questions. Does the elevated [CO2]-induced enhancement of NPP change over time? Does elevated [CO2] change the proportion of C in different plant C pools, or the partitioning of new C, as the stand ages? And, how does elevated [CO2]-induced enhancement of NPP vary with soil N and water availability?
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Elevated [CO2] has the potential to change many aspects of forest ecosystem development and function. We found that elevated [CO2] resulted in a sustained increase in plant biomass production, the magnitude of which was determined by water and, particularly, N availability. The more available these resources were, the greater was the [CO2]-induced enhancement in NPP. Notably, on a relative basis, [CO2]-induced enhancement was mostly invariant with changing P-PET. Thus, the anticipated increase in the relative [CO2]-induced enhancement with increasing moisture limitation (i.e. the amelioration of drought effects by increased [CO2] (e.g. Strain & Bazzaz, 1983) was observed only where N availability was very high. Elevated [CO2] led to increases in NPP (averaging 277 g of C m−2 yr−1) and in standing plant C (averaging 217 g of C m−2 yr−1 greater rate of accumulation), yet did not change the distribution of C among biomass pools or fluxes.
Plant carbon pools and average annual net primary productivity fluxes
The majority of living plant biomass currently in the study ecosystem has been produced since the onset of the experiment (averaging 57% in plots under ambient [CO2] and 62% in plots under elevated [CO2]; Fig. 4d). This means that the vast majority of actively functioning plant tissue (where older wood is nonfunctional or less functional than newer wood) was formed since the commencement of the experiment. Qualitatively, our findings regarding the effects of elevated [CO2] on standing plant biomass and NPP are not fundamentally different from previous assessments at this site (e.g. Hamilton et al., 2002; Schäfer et al., 2003; Finzi et al., 2006). At the treatment level, elevated [CO2] significantly increased NPP and standing plant C, and the enhancement of NPP was maintained over time. However, correction of the systematic underestimation of tree height, and the consequently substantial underestimates of standing biomass and NPP (e.g. DeLucia et al., 1999, 2002; Hamilton et al., 2002; Schäfer et al., 2003; McCarthy et al., 2006a), bring the stand in line with observations of NPP and standing biomass in similar stands in the North Carolina Piedmont region (e.g. Kinerson et al., 1977), as well as moderating what was believed to be a sharp decline in NPP with stand age (Finzi et al., 2006). Furthermore, accurate quantities of plant C pools and fluxes are critical for closing ecosystem C and N budgets in both [CO2] treatments, and are essential for testing and constraining models intended to predict the effect of elevated [CO2] on forest ecosystems.
Interaction effects of [CO2] with nitrogen and water availabilities
In the absence of additional information, initial standing biomass has sometimes been used as a covariate to account for the impact of initial conditions on later effects of elevated [CO2]; however this is likely to be less appropriate for long-term studies in which trees are no longer experiencing exponential growth. It is more desirable to identify the causes of spatial differences and to employ those to interpret the effects of [CO2]. Thus, by extending earlier work linking NPP to net N mineralization (Finzi et al., 2002), this study shows that the N-availability index – statistically interchangeable with initial plant biomass (Fig. 6) – explains much of the spatial variation in NPP at this site and strongly determines the response of NPP to elevated [CO2] (Fig. 7a). The positive interaction with elevated [CO2] results in progressively smaller absolute enhancements of stand NPP as available N decreases. In the extreme, very low availability of nutrients (e.g. in P. taeda on sandy soils and Picea abies on sandy glacial till), have resulted in no observable response to elevated [CO2] (Oren et al., 2001; Ward et al., 2008). In both of these studies, significant [CO2]-induced responses were observed in fertilized trees.
Unsurprisingly we also found that water availability, here represented as growing season P-PET, explained much of the remaining interannual variability in productivity within each treatment (Fig. 7b). This is consistent with previous analysis of factors driving inter-annual variation in pine basal area increment (BAI), as well as previous multivariate analyses showing significant, positive effects of precipitation on NPP under ambient and elevated [CO2] at this site (Finzi et al., 2006; Moore et al., 2006). When we combined the responses of NPP to N and P-PET to assess the effect of varying both N and water availability on the elevated [CO2]-induced enhancement of stand NPP (Fig. 7), we found on an absolute basis, [CO2]-induced enhancement increased with increasing N and P-PET, while on a relative basis, [CO2]-induced enhancement was mostly invariant with changing P-PET. This relative response contrasts with the finding that [CO2]-induced relative enhancement of BAI was strongly related to growing season P, mean temperature and VPD (Moore et al., 2006), the latter two variables positively related to PET. Basal area increments are just one component of stand level NPP, so the disparity in results between BAI and NPP could be caused by the nonlinear increase in tree biomass with increasing tree diameter, and the nonstem biomass components, which are likely to have differential sensitivity to environmental drivers. Two years of our study (2002 and 2003) exhibited NPP that was seemingly decoupled from the current year’s water availability (P-PET). While we have no measure of nonstructural carbohydrates, it seems likely that depletion of these reserves (through drought and ice storm) could have resulted in the below-average NPP observed in these years.
Early conceptual models predicted that relative [CO2]-induced enhancement would increase with increasing nutrient availability and decreasing water availability, such that ecosystems with high water availability and low nutrient availability should be virtually unresponsive to elevated [CO2], and ecosystems with low water availability and high nutrient availability should have the greatest response (e.g. Strain & Bazzaz, 1983). In forests, subsequent data has supported the predictions regarding N availability (Oren et al., 2001; Nowak et al., 2004). By contrast, the projections of greater relative enhancement with decreasing water availability have largely not been borne out by data, with enhancement in forests actually increasing with precipitation (Nowak et al., 2004). Our results add to the very few that quantify the important role that both nutrient and water availability are expected to have in facilitating forest productivity response to elevated [CO2].
Plant carbon partitioning
Our findings of pine standing biomass distribution of 67% to stem, 10% to branches, 18% to roots and 4% to foliage (at age 21 yr), closely match the expected proportions for loblolly pine of ≥ 15 yr, of 65–70% to stem, 10% to branches, 15–20% to roots and 3–5% to foliage (Schultz, 1997). Unlike many assessments of ecosystem C pools and fluxes, this study also captured partitioning to reproductive organs. Although reproductive structures currently represent less than 1% of the total annual C partitioned at the Duke FACE site Table S2), reproduction in loblolly pine was significantly enhanced in plots under high [CO2] and may indicate long-term ecosystem consequences for forest composition (e.g. LaDeau & Clark, 2001, 2006). Similarly, although allocation to mycorrhizae has been estimated to be only approx. 5% of NPP in this forest (K. K. Treseder, unpublished data), significant increases in ectomycorrhizal colonization under elevated [CO2] (Garcia et al., 2008; Pritchard et al., 2008b) are likely to be an important factor contributing to increased NPP under elevated [CO2].
The results from other FACE studies have been mixed with regard to whether elevated [CO2] causes substantial shifts in the proportion of C in various plant pools and whether there is a shift in the partitioning patterns of new C. The L. styraciflua plantation at the ORNL FACE site showed a distinct shift, from up to 80% of the extra NPP induced by [CO2] partitioned to slow pools (wood) during the early phase of the experiment, to only 25% after 3 yr (with the remainder partitioned to fine roots; Norby et al., 2002). Similarly, in the last year of the first rotation in the POP-EUROFACE experiment on Populus species, root pools were increased relatively more under elevated [CO2] than were aboveground woody components (Gielen et al., 2005). However, the root-to-shoot ratio was unchanged, and the fraction of NPP allocated to woody aboveground biomass was high, ranging (among species) from 53 to 67% (Calfapietra et al., 2003; Gielen et al., 2005). Unlike the first rotation, in which the relative accumulation of biomass in stems and roots did not change, during the second (coppice) rotation of Populus species at POP-EUROFACE, elevated [CO2] resulted in greater C accumulation in branches and less accumulation in stems as compared to trees under ambient [CO2]; the ratio of aboveground and belowground biomass remained the same (Liberloo et al., 2006). In contrast, when grow from the start under elevated [CO2], neither the fraction of standing biomass in various pools, nor the partitioning of NPP of Populus tremuloides was changed by elevated [CO2] (King et al., 2005). These differing outcomes suggest that elevated [CO2] does not have a uniform effect on allocation, but rather must be considered in conjunction with other site factors, as reflected, for example, in leaf area index (Palmroth et al., 2006). Additionally, practical approaches to estimating biomass may also constrain the ability to detect some changes in partitioning: in our present study, we can only identify resource-induced changes in partitioning to branches and coarse roots when they are reflected in changes in height or diameter.
Plant C partitioning is the outcome of many processes that are influenced by both internal and external factors (Dewar, 1993; Cannell & Dewar, 1994), and is frequently poorly resolved, even under ambient [CO2] conditions (Litton et al., 2007). However, modeling and empirical advances have been made in some aspects of ecosystem C partitioning. A recent resurgence in optimization models has shown that these models can reproduce measured allocation patterns in current and global change settings (Dewar et al., 2009; Franklin et al., 2009). These studies accurately predicted the quantities of fine root allocation at Duke and ORNL FACE sites, capturing their different partitioning patterns (Franklin et al., 2009). Furthermore, a recent analysis of total belowground C allocation (TBCA) across these four forest FACE sites demonstrated significant, inverse relationships between TBCA and leaf area index and between TBCA and NPP (Palmroth et al., 2006), with a higher fraction of the [CO2]-enhanced NPP allocated belowground where leaf area and NPP are low.
A recent review of plant responses to elevated [CO2] calls for forest FACE experiments to be analyzed with respect to factors driving variation in intrasite growth signals, over as many years as possible, with the recognition that broad averages of elevated [CO2] effects on the C cycle are dependent primarily on the frequency of representation of particular conditions in the literature (Körner, 2006). Here we show that elevated [CO2] may significantly increase the rate of biomass production and the rate of ecosystem-level C storage. However, we also show that NPP enhancement is highly dependent on the availability of other growth resources. Thus, we add our findings to a growing body of literature suggesting that the rate at which extra C will be sequestered with increasing atmospheric [CO2] would greatly depend on the spatial and temporal distributions of other growth resources.