CO2 enhancement of forest productivity constrained by limited nitrogen availability

Abstract

Stimulation of terrestrial plant production by rising CO(2) concentration is projected to reduce the airborne fraction of anthropogenic CO(2) emissions. Coupled climate-carbon cycle models are sensitive to this negative feedback on atmospheric CO(2), but model projections are uncertain because of the expectation that feedbacks through the nitrogen (N) cycle will reduce this so-called CO(2) fertilization effect. We assessed whether N limitation caused a reduced stimulation of net primary productivity (NPP) by elevated atmospheric CO(2) concentration over 11 y in a free-air CO(2) enrichment (FACE) experiment in a deciduous Liquidambar styraciflua (sweetgum) forest stand in Tennessee. During the first 6 y of the experiment, NPP was significantly enhanced in forest plots exposed to 550 ppm CO(2) compared with NPP in plots in current ambient CO(2), and this was a consistent and sustained response. However, the enhancement of NPP under elevated CO(2) declined from 24% in 2001-2003 to 9% in 2008. Global analyses that assume a sustained CO(2) fertilization effect are no longer supported by this FACE experiment. N budget analysis supports the premise that N availability was limiting to tree growth and declining over time--an expected consequence of stand development, which was exacerbated by elevated CO(2). Leaf- and stand-level observations provide mechanistic evidence that declining N availability constrained the tree response to elevated CO(2); these observations are consistent with stand-level model projections. This FACE experiment provides strong rationale and process understanding for incorporating N limitation and N feedback effects in ecosystem and global models used in climate change assessments.

Fig. 1.

Tree growth responses to elevated CO₂. NPP [kilograms dry matter (DM) per square meter land area per year] data are the means of three aCO₂ plots (open symbols) and two eCO₂ plots (solid symbols) ± SEM. The number at each point is the percentage increase under eCO₂. Statistical information is given in SI Materials and Methods.

Fig. 2.

Growth response to nitrogen addition. Responses in the N fertilizer experiment (dashed lines) are compared with responses in the FACE experiment (solid lines). Elevated CO₂ (solid circles) caused a significant increase in wood increment in the first year after treatment initiation (1998), but the response diminished in subsequent years and in later years was not statistically different from FACE controls (open circles). N fertilization (shaded squares) caused an immediate and sustained increase in wood increment compared with unfertilized plots (open squares) (P < 0.001).

Fig. 3.

Relationship of canopy parameters to NPP. (A) N concentration in leaves throughout the canopy of each plot after canopy expansion was complete in July or August of each year. The arrow indicates onset of the CO₂ treatments. (B) The linear relationship between NPP and foliar [N], excluding data from 1998 to 1999 (x and + symbols). (C) Leaf area duration (m² leaf × d·m⁻² ground). (D) NPP increased with increasing LAD in aCO₂ but there was no significant relationship between NPP and LAD in eCO₂. (E) LMA, leaf mass per unit area (g DM/m² leaf area) averaged over the canopy. (F) Linear relationships between NPP and LMA. (G) Total N content of canopy at seasonal peak leaf area (g N/m² ground area). (H) Linear relationship between NPP and canopy N. A, C, E, and G data are the means of three aCO₂ plots (open symbols, dashed black lines) and two eCO₂ plots (solid symbols, solid colored lines) ± SEM. B, D, F, and H data are values for each plot–year combination in aCO₂ (open symbols) and eCO₂ (solid symbols) from 1998 to 2008 with regression lines as indicated. Statistical information is given in SI Materials and Methods.

Fig. 4.

Nitrogen availability. (A) The δ¹⁵N of freshly fallen leaf litter (35), which is an indicator of N availability, declined significantly through time, and the decline in eCO₂ was significantly steeper than that in aCO₂. (B) Annual N uptake to aboveground tree parts per unit ground area. N uptake declined through time, but there was no significant difference between treatments. Data shown are the means of three aCO₂ plots (open symbols, dotted black regression line) and two eCO₂ plots (solid symbols, solid colored regression line) ± SEM. Statistical information is given in SI Materials and Methods.