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CO2 Enhancement of Forest Productivity Constrained by Limited Nitrogen Availability

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CO2 Enhancement of Forest Productivity Constrained by Limited Nitrogen Availability CO2 enhancement of forest productivity constrained by limited nitrogen availability Richard J. Norbya,1, Jeffrey M. Warrena, Colleen M. Iversena, Belinda E. Medlynb, and Ross E. McMurtriec aEnvironmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37830; bDepartment of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia; and cSchool of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia Edited by William H. Schlesinger, Cary Institute of Ecosystem Studies, Millbrook, NY, and approved October 6, 2010 (received for review May 9, 2010) ± Stimulation of terrestrial plant production by rising CO2 concentra- creased by 23 2% in response to atmospheric CO2 enrichment to tion is projected to reduce the airborne fraction of anthropogenic 550 ppm (7). Substantial uncertainty remains, however, because of CO2 emissions. Coupled climate–carbon cycle models are sensitive the expectation that feedbacks through the nitrogen (N) cycle will – to this negative feedback on atmospheric CO2, but model projec- reduce the CO2 stimulation of NPP (8 10). These feedbacks were tions are uncertain because of the expectation that feedbacks not included in the AR4 models and heretofore have not been fi through the nitrogen (N) cycle will reduce this so-called CO2 fertil- con rmed by CO2-enrichment experiments in forests (11). How- ization effect. We assessed whether N limitation caused a reduced ever, N feedbacks have been observed to diminish the CO2 effect stimulation of net primary productivity (NPP) by elevated atmo- on biomass accumulation in nutrient-poor grasslands (12), and spheric CO2 concentration over 11 y in a free-air CO2 enrichment severely N-limited forests show little response to eCO2 (13). (FACE) experiment in a deciduous Liquidambar styraciflua (sweet- To reduce the large uncertainties in climate–C-cycle projec- gum) forest stand in Tennessee. During the first 6 y of the exper- tions, C-cycle models must be constrained by observational data iment, NPP was significantly enhanced in forest plots exposed to (3). Forests, which have the capacity to sequester C from the at- 550 ppm CO2 compared with NPP in plots in current ambient CO2, mosphere in long-lived biomass and soil pools, are an especially and this was a consistent and sustained response. However, the important terrestrial C sink (1). However, few forest experiments enhancement of NPP under elevated CO2 declined from 24% in have been of long enough duration to determine whether an ob- 2001–2003 to 9% in 2008. Global analyses that assume a sustained served stimulation of NPP, which can lead to increased C se- CO2 fertilization effect are no longer supported by this FACE ex- questration, would be sustained through time. The Oak Ridge periment. N budget analysis supports the premise that N availabil- FACE experiment (14, 15) exposed replicate plots in an estab- ity was limiting to tree growth and declining over time —an ex- lished sweetgum (Liquidambar styraciflua) plantation forest to an pected consequence of stand development, which was exacerbated atmosphere with ∼550 ppm CO2 continuously during the 1998– by elevated CO2. Leaf- and stand-level observations provide mech- 2009 growing seasons; here we discuss the results of 11 y of CO2 anistic evidence that declining N availability constrained the tree enrichment. Results from the first 6 y of the experiment indicated response to elevated CO2; these observations are consistent with that NPP was significantly enhanced by eCO2 (Fig. 1) and that this stand-level model projections. This FACE experiment provides was a consistent and sustained response (7). There was little en- strong rationale and process understanding for incorporating N hancement of aboveground wood production (Fig. 2); the bulk of limitation and N feedback effects in ecosystem and global models the NPP increase occurred as increased fine-root production, used in climate change assessments. especially in the deeper soil profile (16). Increased NPP was as- sociated with greater C input to soil (17) and a gain in soil C (18), CO2 fertilization | free air CO2 enrichment | global carbon cycle | and it was this 6-y dataset that was used in a synthesis of NPP sweetgum | coupled climate-carbon cycle models responses in FACE experiments (7). Now, with 11 y of data, our analysis must be revised. olicy decisions to mitigate climate change require dependable Results Ppredictions of the forcings and feedbacks between the terres- trial biosphere and the climate (1). Currently, climate models that The enhancement of NPP under eCO2 relative to current ambient – are coupled to terrestrial and oceanic carbon (C)-cycle models CO2 (aCO2) declined from 24% in 2001 2003 to 9% in 2008, and fi P > simulate a positive feedback to climate change such that the air- there was no signi cant enhancement ( 0.18) in any year after 2004 (Fig. 1). During this period, NPP in aCO2 was diminished by borne fraction of anthropogenic CO2 emissions increases with, and 2 2 amplifies, climatic warming (1). However, the uncertainty in these 47%, from 2.1 kg dry matter/m in 2002 to 1.1 kg/m in 2008. The projections is high, largely because of uncertainty in the offsetting loss in NPP response to eCO2 was entirely accounted for by changes in fine-root production. negative feedback that may occur if stimulation of terrestrial plant Given the speculation that feedbacks through the N cycle production by rising CO concentration increases land C storage 2 could result in the loss of response to eCO , we tested whether our and thereby reduces the airborne fraction of anthropogenic CO 2 2 sweetgum forest was N limited by adding N fertilizer to the sweet- emissions. Coupled climate–C-cycle models, including those used gum plantation adjacent to the FACE experiment. N additions in the Intergovernmental Panel on Climate Change Fourth As- resulted in an immediate increase in NPP; much of the increase in sessment Report (AR4) (2), are sensitive to this negative feedback NPP was due to greater aboveground production, resulting in a de- on atmospheric CO2 (3). For example, dynamic global vegetation crease in relative allocation to fine roots (19). This fertilizer re- models (4) simulate an increased terrestrial C sink resulting from the physiological responses of plants to elevated atmospheric CO2 concentration (eCO2), and when coupled to climate models, in- Author contributions: R.J.N., J.M.W., and C.M.I. designed research; R.J.N., J.M.W., and C. clusion of the CO2 fertilization effect slows the increase in atmo- M.I. performed research; R.J.N., J.M.W., C.M.I., B.E.M., and R.E.M. analyzed data; and R.J. spheric CO2 and the trajectory of climatic warming (5). The N. wrote the paper. representation of the so-called CO2 fertilization effect in the 11 The authors declare no conflict of interest. models used in AR4 and subsequent models (2, 5, 6) was broadly This article is a PNAS Direct Submission. consistent with experimental evidence available at that time from 1To whom correspondence should be addressed. E-mail: [email protected]. four free-air CO2 enrichment (FACE) experiments, which in- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. dicated that net primary productivity (NPP) of forests was in- 1073/pnas.1006463107/-/DCSupplemental. 19368–19373 | PNAS | November 9, 2010 | vol. 107 | no. 45 www.pnas.org/cgi/doi/10.1073/pnas.1006463107 Downloaded by guest on September 29, 2021 year), leaf mass per unit area (LMA), and total canopy N con- tent. LAD varied year to year without any clear trend over time and with no effect of [CO2] (Fig. 3C). NPP increased with LAD in aCO2, but there was no significant relationship between NPP and LAD in eCO2 (Fig. 3D). LMA increased during the exper- iment (Fig. 3E), and NPP was inversely correlated with LMA (Fig. 3F). Canopy N content did not exhibit any clear trend through time except for a decline over the last 3 y (Fig. 3G), but NPP was nevertheless correlated with canopy N (Fig. 3H). The influences of LAD, LMA, and canopy N on NPP were small compared with that of foliar [N]. In a multivariate regression framework, foliar [N] was the only significant predictor of NPP in eCO2, accounting for 73% of the variation. In aCO2 foliar [N] explained 57% of the variation in NPP, and LAD explained an additional 15%. Light-saturated photosynthetic rates were significantly greater (P < 0.05) at eCO2 than at aCO2 in 1999 (means ± SEM were − − − − Fig. 1. Tree growth responses to elevated CO2. NPP [kilograms dry matter 14.5 ± 1.8 μmol·m 2·s 1 vs. 10.4 ± 1.0 μmol·m 2·s 1) (21). (DM) per square meter land area per year] data are the means of three aCO2 ± However, photosynthesis was lower in both treatments in 2008, plots (open symbols) and two eCO2 plots (solid symbols) SEM. The number fi ± at each point is the percentage increase under eCO . Statistical information and there was no longer a signi cant stimulation by eCO2 (7.6 2 μ · −2· −1 ± μ · −2· −1 P > is given in SI Materials and Methods. 0.7 mol m s vs. 6.4 0.7 mol m s , 0.26). Reduc- tions in leaf photosynthesis through time and with CO2 treat- ment reflect differences in the parameters of photosynthetic sponse was sustained even as tree growth in control plots (and in biochemistry, Vcmax (the maximum rate of carboxylation) and the adjacent FACE plots) was declining (Fig. 2). Jmax (maximum rate of electron transport at saturating irradi- Canopy-averaged foliar [N] in the FACE experiment declined ance.) Foliar N per unit leaf area, Narea, in the upper 2 m of the over time in both aCO2 and eCO2 (Fig.
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