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Title: Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2

Abstract

Forest ecosystems are important sinks for rising concentrations of atmospheric CO2. In a previous data synthesis of four forest FACE experiments (1), forest net primary production (NPP) increased by 23 2% when the forests were grown under atmospheric concentrations of CO2 predicted for the latter half of this century. Because nitrogen (N) availability commonly limits forest productivity, more N must be taken up from the soil and/or the N already assimilated by trees must be used more efficiently to support high rates of forest productivity under elevated CO2. Biogeochemical models predict that increases in forest NPP under elevated CO2 in N-limited ecosystems result in a significant increase in N-use efficiency (NUE), and that additional uptake of N by trees under elevated CO2 is only possible in ecosystems where N is not limiting. Here, experimental evidence demonstrates that patterns of N uptake and NUE under elevated CO2 differed from that predicted by biogeochemical models. The uptake of N increased under elevated CO2 at the Rhinelander, Duke and Oak Ridge National Laboratory (ORNL) FACE sites, yet fertilization studies at the Duke and ORNL FACE sites showed that tree growth and forest NPP were strongly limited by N availability. By contrast, NUE increasedmore » under elevated CO2 only at the POP-EUROFACE site where fertilization studies showed that N was not limiting to tree growth. In reviewing data from the forest FACE experiments, we suggest that some combination of increasing fine root production, increased rates of soil organic matter (SOM) decomposition, and increased allocation of carbon (C) to mycorrhizal fungi is likely to account for greater N uptake under elevated CO2 at the forest FACE sites. To accurately forecast the response of forest ecosystems to rising concentrations of atmospheric CO2, biogeochemical models must be reformulated to allow C transfers belowground that result in additional N uptake under elevated CO2.« less

Authors:
 [1];  [2];  [3];  [4];  [2];  [5];  [6];  [2];  [5];  [4]
  1. Boston University
  2. ORNL
  3. University of Tuscia
  4. University of Antwerp
  5. Duke University
  6. U.S. Department of Agriculture Forest Service
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Oak Ridge National Environmental Research Park
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
932095
DOE Contract Number:
DE-AC05-00OR22725
Resource Type:
Journal Article
Resource Relation:
Journal Name: Proceedings of the National Academy of Sciences; Journal Volume: 104; Journal Issue: 35
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; AVAILABILITY; CARBON DIOXIDE; ECOSYSTEMS; EFFICIENCY; FERTILIZATION; FORESTS; FUNGI; NITROGEN; ORGANIC MATTER; ORNL; PRODUCTION; PRODUCTIVITY; SOILS; SYNTHESIS; TREES; CO2; global change; nitrogen; net primary productivity; nitrogen use efficiency

Citation Formats

Finzi, Adrien C, Norby, Richard J, Califapietra, Carlo, Gielen, Birgit, Iversen, Colleen M, Jackson, Robert B, Kubiske, Mark E, Childs, Joanne, Schlesinger, William H, and Ceulemans, Reinhart. Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. United States: N. p., 2007. Web. doi:10.1073/pnas.0706518104.
Finzi, Adrien C, Norby, Richard J, Califapietra, Carlo, Gielen, Birgit, Iversen, Colleen M, Jackson, Robert B, Kubiske, Mark E, Childs, Joanne, Schlesinger, William H, & Ceulemans, Reinhart. Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. United States. doi:10.1073/pnas.0706518104.
Finzi, Adrien C, Norby, Richard J, Califapietra, Carlo, Gielen, Birgit, Iversen, Colleen M, Jackson, Robert B, Kubiske, Mark E, Childs, Joanne, Schlesinger, William H, and Ceulemans, Reinhart. Mon . "Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2". United States. doi:10.1073/pnas.0706518104.
@article{osti_932095,
title = {Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2},
author = {Finzi, Adrien C and Norby, Richard J and Califapietra, Carlo and Gielen, Birgit and Iversen, Colleen M and Jackson, Robert B and Kubiske, Mark E and Childs, Joanne and Schlesinger, William H and Ceulemans, Reinhart},
abstractNote = {Forest ecosystems are important sinks for rising concentrations of atmospheric CO2. In a previous data synthesis of four forest FACE experiments (1), forest net primary production (NPP) increased by 23 2% when the forests were grown under atmospheric concentrations of CO2 predicted for the latter half of this century. Because nitrogen (N) availability commonly limits forest productivity, more N must be taken up from the soil and/or the N already assimilated by trees must be used more efficiently to support high rates of forest productivity under elevated CO2. Biogeochemical models predict that increases in forest NPP under elevated CO2 in N-limited ecosystems result in a significant increase in N-use efficiency (NUE), and that additional uptake of N by trees under elevated CO2 is only possible in ecosystems where N is not limiting. Here, experimental evidence demonstrates that patterns of N uptake and NUE under elevated CO2 differed from that predicted by biogeochemical models. The uptake of N increased under elevated CO2 at the Rhinelander, Duke and Oak Ridge National Laboratory (ORNL) FACE sites, yet fertilization studies at the Duke and ORNL FACE sites showed that tree growth and forest NPP were strongly limited by N availability. By contrast, NUE increased under elevated CO2 only at the POP-EUROFACE site where fertilization studies showed that N was not limiting to tree growth. In reviewing data from the forest FACE experiments, we suggest that some combination of increasing fine root production, increased rates of soil organic matter (SOM) decomposition, and increased allocation of carbon (C) to mycorrhizal fungi is likely to account for greater N uptake under elevated CO2 at the forest FACE sites. To accurately forecast the response of forest ecosystems to rising concentrations of atmospheric CO2, biogeochemical models must be reformulated to allow C transfers belowground that result in additional N uptake under elevated CO2.},
doi = {10.1073/pnas.0706518104},
journal = {Proceedings of the National Academy of Sciences},
number = 35,
volume = 104,
place = {United States},
year = {Mon Jan 01 00:00:00 EST 2007},
month = {Mon Jan 01 00:00:00 EST 2007}
}
  • Elevated CO2 increases intrinsic water use efficiency (WUEi) of forests, but the magnitude of this effect and its interaction with climate is still poorly understood. We combined tree ring analysis with isotope measurements at three Free Air CO2 Enrichment (FACE, POP-EUROFACE, in Italy; Duke FACE in North Carolina and ORNL in Tennessee, USA) sites, to cover the entire life of the trees. We used 13C to assess carbon isotope discrimination ( 13C ci/ca) and changes in WUEi, while direct CO2 effects on stomatal conductance were explored using 18O as a proxy. Across all the sites, elevated CO2 increased 13C-derived WUEimore » on average by 73% for Liquidambar styraciflua, 77% for Pinus taeda and 75% for Populus sp., but through different ecophysiological mechanisms. Our findings provide a robust means of predicting WUEi responses from a variety of tree species exposed to variable environmental conditions over time, and species-specific relationships that can help modeling elevated CO2 and climate impacts on forest productivity, carbon and water balances.« less
  • The Progressive Nitrogen Limitation (PNL) hypothesis suggests that ecosystems in a CO2-enriched atmosphere will sequester C and N in long-lived biomass and soil organic pools, thereby limiting available N and constraining the continued response of net primary productivity to elevated [CO2]. Here, we present a six-year record of N dynamics of a sweetgum (Liquidambar styraciflua) stand exposed to elevated [CO2] in the free-air CO2 enrichment (FACE) experiment at Oak Ridge, Tennessee, USA. We also evaluate the concept of PNL for this ecosystem from the perspective of N uptake, content, distribution, and turnover, and N-use efficiency. Leaf N content was 11%more » lower on a leaf mass basis (NM) and 7% lower on a leaf area basis (N{sub A}) in CO2-enriched trees. However, there was no effect of [CO2] on total canopy N content. Resorption of N during senescence was not altered by [CO2], so NM of litter, but not total N content, was reduced. The NM of fine roots was not affected, but the total amount of N required for fine-root production increased significantly, reflecting the large stimulation of fine-root production in this stand. Hence, total N requirement of the trees was higher in elevated [CO2], and the increased requirement was met through an increase in N uptake rather than increased retranslocation of stored reserves. Increased N uptake was correlated with increased net primary productivity (NPP). N-use efficiency, however, did not change with CO2 enrichment because increased N productivity was offset by lower mean residence time of N in the trees. None of the measured responses of plant N dynamics in this ecosystem indicated the occurrence of PNL, and the stimulation of NPP by elevated [CO2] was sustained for the first six years of the experiment. Although there are some indications of developing changes in the N economy, the N supply in the soil at this site may be sufficient to meet an increasing demand for available N, especially as the roots of CO2-enriched trees explore deeper in the soil profile.« less
  • Despite the importance of nitrogen (N) limitation of forest carbon (C) sequestration at rising atmospheric CO2 concentration, the mechanisms responsible are not well understood. To elucidate the interactive effects of elevated CO2 (eCO2) and soil N availability on forest productivity and C allocation, we hypothesized that 1) trees maximize fitness by allocating N and C to maximize their net growth, and 2) that N uptake is controlled by root exploration for N. We tested this model using data collected in FACE sites dominated by evergreen (Pinus taeda; Duke Forest) and deciduous (Liquidambar styraciflua; Oak Ridge National Laboratory ORNL) trees. Themore » model explained 80-95% of variation in productivity and N-uptake data among eCO2, N fertilization and control treatments over six years. The model explains why fine-root production increased, and why N uptake increased despite reduced soil N availability under eCO2 at ORNL and Duke. In agreement with observations at other sites, soil N availability reduced below a critical level diminishes all eCO2 responses. At Duke, a negative feedback between reduced soil N availability and N uptake counteracted progressive reduction in soil N availability at eCO2. At ORNL, decreasing soil N availability was perpetuated as it generated no reduction in N uptake, due to strongly increased production of fast turnover fine-roots. This implies that species with fast root turnover could be more prone to progressive N limitation of carbon sequestration in woody biomass than species with slow root turnover, such as evergreens.« less
  • The impacts of extreme weather events on water-carbon (C) coupling and ecosystem-scale water use efficiency (WUE) over a long term are poorly understood. We analyzed the changes in ecosystem water use efficiency (WUE) from 10 years of eddy-covariance measurements (2004-2013) over an oak-dominated temperate forest in Ohio, USA. The aim was to investigate the long-term response of ecosystem WUE to measured changes in site-biophysical conditions and ecosystem attributes. The oak forest produced new plant biomass of 2.5 +/- 0.2 gC kg(-1) of water loss annually. Monthly evapotranspiration (ET) and gross ecosystem production (GEP) were tightly coupled over the 10-year studymore » period (R-2=0.94). Daily WUE had a linear relationship with air temperature (T-a) in low-temperature months and a unimodal relationship with T-a in high-temperature months during the growing season. On average, daily WUE ceased to increase when T-a exceeded 22 degrees C in warm months for both wet and dry years. Monthly WUE had a strong positive linear relationship with leaf area index (LAI), net radiation (R-n), and T-a and weak logarithmic relationship with water vapor pressure deficit (VPD) and precipitation (P) on a growing-season basis. When exploring the regulatory mechanisms on WUE within each season, spring LAI and P, summer R-n and T-a, and autumnal VPD and R-n were found to be the main explanatory variables for seasonal variation in WUE. The model developed in this study was able to capture 78% of growing-season variation in WUE on a monthly basis. The negative correlation between WUE and A in spring was mainly due to the high precipitation amounts in spring, decreasing GEP and WUE when LAI was still small, adding ET being observed to increase with high levels of evaporation as a result of high SWC in spring. Summer WUE had a significant decreasing trend across the 10 years mainly due to the combined effect of seasonal drought and increasing potential and available energy increasing ET, but decreasing GEP in summer. We concluded that seasonal dynamics of the interchange between precipitation and drought status of the system was an important variable in controlling seasonal WUE in wet years. In contrast, despite the negative impacts of unfavorable warming, available groundwater and an early start of the growing season were important contributing variables in high seasonal GEP, and thus, high seasonal WUE in dry years. (C) 2015 Elsevier B.V. All rights reserved.« less