Contributions of nitrogen deposition and forest regrowth to terrestrial carbon uptake
© Churkina et al; licensee BioMed Central Ltd. 2007
Received: 27 March 2007
Accepted: 29 May 2007
Published: 29 May 2007
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© Churkina et al; licensee BioMed Central Ltd. 2007
Received: 27 March 2007
Accepted: 29 May 2007
Published: 29 May 2007
The amount of reactive nitrogen deposited on land has doubled globally and become at least five-times higher in Europe, Eastern United States, and South East Asia since 1860 mostly because of increases in fertilizer production and fossil fuel burning. Because vegetation growth in the Northern Hemisphere is typically nitrogen-limited, increased nitrogen deposition could have an attenuating effect on rising atmospheric CO2 by stimulating the vegetation productivity and accumulation of carbon in biomass.
This study shows that elevated nitrogen deposition would not significantly enhance land carbon uptake unless we consider its effects on re-growing forests. Our results suggest that nitrogen enriched land ecosystems sequestered 0.62–2.33 PgC in the 1980s and 0.75–2.21 PgC in the 1990s depending on the proportion and age of re-growing forests. During these two decades land ecosystems are estimated to have absorbed 13–41% of carbon emitted by fossil fuel burning.
Although land ecosystems and especially forests with lifted nitrogen limitations have the potential to decelerate the rise of CO2 concentrations in the atmosphere, the effect is only significant over a limited period of time. The carbon uptake associated with forest re-growth and amplified by high nitrogen deposition will decrease as soon as the forests reach maturity. Therefore, assessments relying on carbon stored on land from enhanced atmospheric nitrogen deposition to balance fossil fuel emissions may be inaccurate.
The global climate is expected to change in response to rising concentrations of atmospheric carbon dioxide (CO2), because CO2 in the atmosphere traps heat. The magnitude of this change depends on the rate of CO2 emissions from human activities as well as on carbon uptake by oceans and land. Carbon dioxide fertilization, climate change, nitrogen deposition and land management can enhance carbon uptake on land. A globally significant carbon sink in 1980's-1990's in northern extratropical regions  was inferred from variations in atmospheric CO2 concentrations. Although this sink was attributed mostly to forest ecosystems [2–5], the magnitude and cause of this sink remain uncertain. Population growth, industrial expansion, and political changes lead to exponentially increasing deposition of reactive nitrogen on land and re-growth of forests, which were identified among the major causes of land carbon sink in the Northern Hemisphere.
Nitrogen is a primary limiting nutrient throughout terrestrial ecosystems of mid and high latitudes, and an important limiting nutrient for plant growth throughout subtropical and tropical ecosystems , where phosphorus is a co-limiting or limiting nutrient [7, 8]. Additional nitrogen supply through fertilization and atmospheric deposition could reduce or even remove the nitrogen limitation on carbon uptake. Overload of nitrogen deposited on land can lead to decline of ecosystems. Globally the amount of reactive atmospheric nitrogen inputs increased from 41 TgN/yr in 1950 to 103 TgN/yr in 2000 with proportional increase of deposition on land . One third of the global nitrogen inputs entered the land ecosystems and one tenth the forests. Given the high carbon to nitrogen ratios and long lifetimes of carbon in wood, a most significant effect of nitrogen fertilization is expected in forests.
Did land carbon uptake increase in response to the higher nitrogen depositions during the last few decades? Studies addressing this question agreed on the location of major response – the temperate forests located between 25° and 55° north, but disagree on the magnitude of the response. Based on results from a series of 15N-tracer field experiments, Nadelhoffer et al.  argued that increased inputs of combined nitrogen from atmosphere made a minor contribution to land carbon uptake. Their stoichiometric budget suggested that fertilized temperate forests sequestered only 0.25 PgC per year in addition. In contrast, model based estimates [11, 12] showed significant increases in land carbon uptake. Townsend et al.  estimated an additional carbon uptake by land in the order of 0.3–1.3 PgC per year, using an ecosystem model and spatially explicit nitrogen depositions from fossil fuels burning (NOy). Using the same vegetation model and various predicted spatial distributions of atmospheric nitrogen deposition (including both NOy and NHx), Holland et al.  showed even higher carbon uptake of 1.5–2.0 Pg per year. Forest regrowth was identified as another major driver of elevated carbon uptake in the Northern Hemisphere in 1980–1999. Changing forest management practices lead to increasing fraction of young forests with higher carbon uptake. Depending on the country these young forests were either planted after harvesting or on abandoned agricultural land. Based on forest inventories a carbon sink of 0.11 PgC/yr in Europe and 0.018 PgC/yr in Japan was primarily attributed to regrowth of young forests [2, 3]. In China and the United States both forest regrowth and afforestation lead to carbon sink of 0.03 PgC/yr  and 0.11–0.15 PgC/yr [5, 13] respectively. Russian forests have been reported as a highly variable carbon sink (0.06–0.3 Pg C/yr) during those decades . Although the increased uptake of CO2 caused by forest regrowth and afforrestation is relatively undisputed, the relative roles of climate change or land management responsible for this increase has not been defined. In addition, atmospheric nitrogen deposition was exponentially increasing during the same time period. Was nitrogen fertilization leading to a faster forest re-growth and hence to an increased land carbon uptake?
In this study we investigate combined effect of increased nitrogen deposition and forest re-growth on land carbon uptake. We use results of biogeochemical model simulations to show that elevated nitrogen deposition is unlikely to be the major contributor to the increased land carbon sink unless we consider its effects on re-growing forests. The atmospheric nitrogen deposition for 1860–1999 was calculated by the state-of-the-art three dimensional atmospheric chemistry transport model TM3 , which provided spatial distributions of reactive atmospheric nitrogen deposition (NOy and NHx). To assess the effect of enhanced nitrogen deposition on land carbon uptake we used a terrestrial biogeochemical model BIOME-BGC [16–18], which calculates water, carbon, and nitrogen pools dynamics as well as their fluxes. The model considers explicit patterns of nitrogen input and loss from ecosystems (see Methods). To isolate effects of increasing nitrogen deposition we performed model simulations with both increasing CO2 and nitrogen deposition as well as with increasing CO2 and constant nitrogen deposition. We estimate carbon uptake of land ecosystems assuming that temperate forests were at three different growth stages: 'mature', 'middle-aged', and 'young'.
The differences between mature and young forests responses to high nitrogen inputs diminish once re-growing forest matures. Change in land carbon uptake from 1980's to 1990's had opposite trends in simulation with mature and in simulations with re-growing forests. Assuming mature forests our model estimates suggested that in 1990's land absorbed 0.13 Pg of carbon per year more than in 1980's. This increase was associated with rising deposition of reactive nitrogen only (from 80 TgN/yr in 1980's to 95 TgN/yr 1990's). In both simulations with re-growing forests the additional carbon uptake has dropped by 0.24–0.44 PgC/yr from 1980's to 1990's. This drop has occurred because growth of forests was slowing down after the initial stage of fast growth, which was accelerated by higher nitrogen inputs. As the forest ages more biomass is accumulated and ecosystem respiration is increasing. Therefore increased carbon gain in forests can not last forever.
Residual land carbon sink
1980's (Pg C/yr)
1990's (Pg C/yr)
Residual land carbon sink
IPCC 2001 
House et al. 
Additional land carbon uptake due to increased nitrogen deposition (globally)
Townsend et al. 
Holland et al. 
Additional land carbon uptake due to increased nitrogen deposition (temperate forests)
Nadelhoffer et al. 
Would this additional carbon accumulated on land offset the fossil fuel emissions? During 1980–1999 approximately 110 Pg of carbon has been emitted into the atmosphere from fossil fuel burning, industry, and deforestation (EDGAR-HYDE 1.4, ). Our model predicted that increased atmospheric nitrogen deposition had caused 14, 25, and 45 Pg of additional carbon to accumulate on land during the same time period assuming mature, middle-age, and young forests respectively (compared to a case where we assumed pre-industrial levels of reactive nitrogen deposition). Assuming that age structure of the world forests in 1980–1999 was between ages of the mature and young forests used in model's simulations, increased nitrogen deposition could attenuate rising atmospheric CO2 by something between 13% and 41%. The real number lays somewhere in between, most likely closer to the lower limit, since only small fraction of the world forests in 1980's and 1990's were re-growing. Once the forests mature, their ability to take up more carbon will diminish.
Our budget (Table 1) is subject to some uncertainties related to simplified representation of ecosystem processes as well as land use dynamics in our modelling study. First, our model does not include the mechanism for nitrogen uptake through the stomata of leaves. In closed-canopy forests, forest canopies can intercept atmospheric nitrogen and assimilate retained reactive nitrogen from air. This mechanism was not implemented in the model, because it is not clear how significant the proportion of total incoming inorganic nitrogen intercepted by the canopy is. If this proportion is only 16% as estimated for North American forests , then it would not change our results considerably. However if it reaches 40% or more than 90%  and all intercepted nitrogen is taken up by foliage then a nitrogen-induced carbon sink may be higher than estimated in our study. Second, our model does not include transformations of reactive nitrogen in the soil, which may be locked up in soil or cause production of dissolved organic nitrogen and carbon. Experiments [24, 25] suggest that chronic additions of nitrate to terrestrial ecosystems lead to higher leaching of dissolved organic nitrogen and carbon rather than to plant productivity increase. The mechanisms behind formation of these dissolved organic compounds and conditions under which it occurs still have to be understood. Including this feedback may decrease estimates of land carbon uptake in some regions. Third, we assumed that land cover remained constant during 1980–1999. In reality the land cover has been experiencing changes during the last two decades. The estimates of these changes and their locations however are highly uncertain. Forest area was decreasing globally by approximately 2% per decade . In Europe and North America, forest cover increased by approximately 0.14–0.2% per decade [2, 26]. In China forest cover was decreasing by 2.3% per decade according to FAO  and increasing by 1.5% per decade according to Fang . Given these uncertainties in forest cover change, we feel that assumption of constant land cover was acceptable in this study.
This study is a frontier research and the results need some confirmation from an independent modelling effort which may include a more detailed treatment of nitrogen cycle and carbon-nitrogen interactions. In addition to the abovementioned processes the next generation of global biogeochemical models may include the following mechanisms: different fates of NHx and NOy within an ecosystem and corresponding effects on ecosystem dynamics; depression of nitrogen mineralization in soils under increasing atmospheric deposition of nitrogen; "N saturation" effects, with N leaching losses approaching N input rates in forests; effect of available nitrogen on carbon allocation within a plant as well as changing plant and soil C:N ratios under chronic N additions. Given complexity of the nitrogen cycle and limitations of any modelling approach, we have to prioritize processes to be included based on their generality and level of understanding.
In this study we analysed the combined effect of increasing nitrogen deposition and forest re-growth on the global land uptake of carbon. We conclude that elevated nitrogen deposition is unlikely to be the major contributor to the increased land carbon sink unless we consider its effects on re-growing forests. Moreover carbon uptake associated with forest re-growth and amplified by high nitrogen deposition will decrease as soon as forests reach maturity. To refine our estimates of land carbon uptake we would need to know the locations of re-growing forests and their age. We also may need to revise the model's representation of carbon-nitrogen interactions in ecosystems once we better understand different pathways of plant nitrogen uptake, role of nitrogen availability in the allocation of carbon, and formation of dissolved organic nitrogen in soil.
Although fossil fuel burning, intensive agriculture, and forest management increase CO2 emissions to the atmosphere, they can also stimulate land carbon uptake, which partially offsets increasing CO2 from fossil fuel emissions. These secondary effects such as increased nitrogen deposition and re-growth of forests should not be considered as purely beneficial. High nitrogen deposition can lead also to nitrogen saturation which, depending on ecosystem type, can cause forest decline [27, 28] or dramatic increases in export of dissolved organic carbon and nitrogen from forest ecosystems to streams, rivers, lakes, and coastal systems . High NOx emissions lead to ozone production , which can have damaging effects on plant growth.
To assess the effect of enhanced nitrogen deposition and CO2 on European carbon uptake we used a terrestrial biogeochemical model BIOME-BGC (version 4.1.1 with carbon and nitrogen allocation routine from 4.1), which calculates water, carbon, and nitrogen pools dynamics as well as their fluxes on a daily basis[16, 30]. The model is driven by maximum and minimum air temperatures, precipitation, air humidity, and solar radiation data. Carbon dynamics include calculations of the plant growth onset and senescence periods, allocation of assimilates to the different plant organs, mortality as well as litter production, and soil organic matter decomposition. Nitrogen dynamics include calculations of plant and soil microbial demands based on carbon to nitrogen ratios of plant organs, litter, and soil microbial community. The amount of nitrogen available to satisfy these demands is determined by nitrogen deposited from atmosphere, biological nitrogen fixation and nitrogen mineralized during soil organic matter decomposition. Nitrogen loss from ecosystem is determined by the amount of soluble mineral nitrogen available, water outflow, and soil water content.
Possible forest decline caused by high nitrogen inputs were not included in the model, because it was not relevant on the coarse grid scale considered in this study.
The Biome-BGC model was successfully evaluated for a number of hydrological and carbon cycle components [31–33]. In recent years, the model has been corroborated with eddy-covariance data at the sites with high and low deposition of atmospheric nitrogen [17, 18, 34, 35].
The model was parameterized for seven vegetation types: deciduous broadleaf forest, evergreen needleaf forest, evergreen broadleaf forest, evergreen deciduous forest, scrubland, C4 and C3 grasslands. Ecophysiological parameters (e.g. carbon to nitrogen ratios of forest ecosystem's pools) for evergreen needleaf and deciduous broadleaf forests were optimized from field measurements of net carbon fluxes . Parameterizations for evergreen broadleaf forest, deciduous needleaf forest, grasslands, and shrubland were as in White et al. .
All input data were transformed to 1° × 1° spatial resolution and subsequent model simulations were performed at this spatial resolution as well. Input land surface characteristics included digital elevation map, soil texture map, and land cover classification. Since in this study we did not consider land use changes, for all spatially explicit simulations of carbon, nitrogen, and water fluxes, a vegetation map  was held constant.
The model was first run with constant annual atmospheric nitrogen deposition (2 kgN/ha yr, Holland, 1999 #728) and CO2 concentrations (283 ppm) as well as daily climate data from NCEP Reanalysis  for 1948–1957 at a spatial resolution of 1° × 1° until an ecological equilibrium was reached.
We isolated the effects of elevated nitrogen deposition on forests at different succession stages by simulations with CO2 increase, but no nitrogen deposition increase and with both CO2 and nitrogen increases. In each simulation we assumed that forests had the same age distribution.
Between 1860 and 1999, ambient CO2 increased from 283 ppm to 368 ppm. To isolate the effect of increased CO2 on carbon uptake we performed model simulations with nitrogen deposition kept constant at 1860 level and CO2 changing as described above.
To isolate the additional effect of increased nitrogen deposition on carbon uptake we performed model simulations with changing both atmospheric CO2 and nitrogen deposition.
The BIOME-BGC model simulations were driven by the state-of-the-art atmospheric nitrogen deposition for 1860–1999 (Figure 2). Spatial distribution of atmospheric nitrogen deposition was estimated with three dimensional atmospheric chemical transport model TM3 . The estimates included deposition of both NOy and NHx, which were added to get the total atmospheric nitrogen deposition.
These data were produced using the TM3 global chemistry transport model that has a horizontal resolution of 5° longitude and 3.75° latitude, and has 19 vertical levels to 10 hPa. It is driven by six-hourly meteorological data obtained from the European Centre for Medium-Range Weather Forecasting. Mid-1990s deposition rates are based on Rodhe et al.  combining output for reduced and oxidized nitrogen deposition (both wet and dry). Comparisons between modelled and measured deposition rates show model accuracy to be within 50% (and often substantially better). The main sources of error arise from emissions inventories, atmospheric transport, removal, and chemical transformations. The original annual model outputs at decadal time step were transformed to annual outputs at one year time step using linear interpolation for each grid pixel.
We acknowledge support by CARBOEUROPE project (contract number: GOCE-CT-2003–505572), which provided funding for Mona Vetter. We are grateful to Victor Brovkin for helpful comments to the earlier draft of this manuscript. We thank four anonymous reviewers and the handling editor, Dr. Alexandorov, for their constructive suggestions, which helped to improve manuscript significantly.
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.