Alan R. Townsend

Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions

Humans continue to transform the global nitrogen cycle at a record pace, reflecting an increased combustion of fossil fuels, growing demand for nitrogen in agriculture and industry, and pervasive inefficiencies in its use. Much anthropogenic nitrogen is lost to air, water, and land to cause a cascade of environmental and human health problems. Simultaneously, food production in some parts of the world is nitrogen-deficient, highlighting inequities in the distribution of nitrogen-containing fertilizers. Optimizing the need for a key human resource while minimizing its negative consequences requires an integrated interdisciplinary approach and the development of strategies to decrease nitrogen-containing waste.

Nutrient Imbalances in Agricultural Development

Nutrient additions to intensive agricultural systems range from inadequate to excessive—and both extremes have substantial human and environmental costs. Nutrient cycles link agricultural systems to their societies and surroundings; inputs of nitrogen and phosphorus in particular are essential for high crop yields, but downstream and downwind losses of these same nutrients diminish environmental quality and human well-being. Agricultural nutrient balances differ substantially with economic development, from inputs that are inadequate to maintain soil fertility in parts of many developing countries, particularly those of sub-Saharan Africa, to excessive and environmentally damaging surpluses in many developed and rapidly growing economies. National and/or regional policies contribute to patterns of nutrient use and their environmental consequences in all of these situations (1). Solutions to the nutrient challenges that face global agriculture can be informed by analyses of trajectories of change within, as well as across, agricultural systems.

Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems

Human activities have clearly caused dramatic alterations of the terrestrial nitrogen cycle, and analyses of the extent and effects of such changes are now common in the scientific literature. However, any attempt to evaluate N cycling processes within ecosystems, as well as anthropogenic influences on the N cycle, requires an understanding of the magnitude of inputs via biological nitrogen fixation (BNF). Although there have been many studies addressing the microbiology, physiology, and magnitude of N fixation at local scales, there are very few estimates of BNF over large scales. We utilized >100 preexisting published estimates of BNF to generate biome- and global-level estimates of biological N fixation. We also used net primary productivity (NPP) and evapotranspiration (ET) estimates from the Century terrestrial ecosystem model to examine global relationships between these variables and BNF as well as to compare observed and Century-modeled BNF. Our data-based estimates showed a strong positive relationship between ecosystem ET and BNF, and our analyses suggest that while the models simple relationships for BNF predict broad scale patterns, they do not capture much of the variability or magnitude of published rates. Patterns of BNF were also similar to patterns of ecosystem NPP. Our “best estimate” of potential nitrogen fixation by natural ecosystems is ∼195 Tg N yr−1, with a range of 100–290 Tg N yr−1. Although these estimates do not account for the decrease in natural N fixation due to cultivation, this would not dramatically alter our estimate, as the greatest reductions in area have occurred in systems characterized by relatively low rates of N fixation (e.g., grasslands). Although our estimate of BNF in natural ecosystems is similar to previously published estimates of terrestrial BNF, we believe that this study provides a more documented, constrained estimate of this important flux.

Variable effects of nitrogen additions on the stability and turnover of soil carbon

Soils contain the largest near-surface reservoir of terrestrial carbon and so knowledge of the factors controlling soil carbon storage and turnover is essential for understanding the changing global carbon cycle. The influence of climate on decomposition of soil carbon has been well documented, but there remains considerable uncertainty in the potential response of soil carbon dynamics to the rapid global increase in reactive nitrogen (coming largely from agricultural fertilizers and fossil fuel combustion). Here, using 14C, 13C and compound-specific analyses of soil carbon from long-term nitrogen fertilization plots, we show that nitrogen additions significantly accelerate decomposition of light soil carbon fractions (with decadal turnover times) while further stabilizing soil carbon compounds in heavier, mineral-associated fractions (with multidecadal to century lifetimes). Despite these changes in the dynamics of different soil pools, we observed no significant changes in bulk soil carbon, highlighting a limitation inherent to the still widely used single-pool approach to investigating soil carbon responses to changing environmental conditions. It remains to be seen if the effects observed here—caused by relatively high, short-term fertilizer additions—are similar to those arising from lower, long-term additions of nitrogen to natural ecosystems from atmospheric deposition, but our results suggest nonetheless that current models of terrestrial carbon cycling do not contain the mechanisms needed to capture the complex relationship between nitrogen availability and soil carbon storage.

Spatial and Temporal Patterns in Terrestrial Carbon Storage Due to Deposition of Fossil Fuel Nitrogen

Fertilization of the biosphere by nitrogen deposition represents an important connection between atmospheric chemistry and the global carbon cycle. We describe a modeled estimate of terrestrial carbon storage arising from deposition of nitrogen derived from fossil fuels that accounts for spatial distributions in deposition and vegetation types, turnover of plant and soil carbon pools, and the cumulative effects of deposition. Vegetation type has a pronounced effect on C uptake; the combination of high C: N ratios and long lifetimes in wood may create a significant sink in forests, but much of the nitrogen falls on cultivated areas and grasslands, where there is limited capacity for long-term carbon storage. We estimate 1990 net carbon uptake due to deposition of fossil-fuel N to be between 0.3 and 1.3 Pg C/yr (1 Pg = 1015 g), depending on the fraction of C allocated to wood, with a best estimate of 0.44-0.74 Pg/yr. Cumulative C storage since 1845 is estimated to be about 25% of the proposed terrestrial sink for anthropogenic CO2. Continued exposure to high N deposition, however, will decrease the extent of N limitation in terrestrial eco- systems, thereby limiting the persistence of any N-derived carbon sink.

The globalization of N deposition: ecosystem consequences in tropical environments

Human activities have more than doubled the inputs of nitrogen (N) into terrestrial systems globally. The sources and distribution of anthropogenic N, including N fertilization and N fixed during fossil fuel combustion, are rapidly shifting from the temperate zone to a more global distribution. The consequences of anthropogenic N deposition for ecosystem processes and N losses have been studied primarily in N-limited ecosystems in the temperate zone; there is reason to expect that tropical ecosystems, where plant growth is most often limited by some other resource, will respond differently to increasing deposition. In this paper, we assess the likely direct and indirect effects of increasing anthropogenic N inputs on tropical ecosytem processes. We conclude that anthropogenic inputs of N into tropical forests are unlikely to increase productivity and may even decrease it due to indirect effects on acidity and the availability of phosphorus and cations. We also suggest that the direct effects of anthropogenic N deposition on N cycling processes will lead to increased fluxes at the soil-water and soil-air interfaces, with little or no lag in response time. Finally, we discuss the uncertainties inherent in this analysis, and outline future research that is needed to address those uncertainties.

Human health effects of a changing global nitrogen cycle

Changes to the global nitrogen cycle affect human health well beyond the associated benefits of increased food production. Many intensively fertilized crops become animal feed, helping to create disparities in world food distribution and leading to unbalanced diets, even in wealthy nations. Excessive air- and water-borne nitrogen are linked to respiratory ailments, cardiac disease, and several cancers. Ecological feedbacks to excess nitrogen can inhibit crop growth, increase allergenic pollen production, and potentially affect the dynamics of several vector-borne diseases, including West Nile virus, malaria, and cholera. These and other examples suggest that our increasing production and use of fixed nitrogen poses a growing public health risk.

Phosphorus Limitation of Microbial Processes in Moist Tropical Forests: Evidence from Short-term Laboratory Incubations and Field Studies

AbstractAlthough there is a widespread belief that phosphorus (P) limits basic ecosystem processes in moist tropical forests, direct tests of this supposition are rare. At the same time, it is generally believed that P does not limit soil microorganism respiration or growth in terrestrial ecosystems. We used natural gradients in P fertility created by soils of varying age underlying tropical rain forests in southwestern Costa Rica, combined with direct manipulations of carbon (C) and P supply, to test the effects of P availability on the decomposition of multiple forms of C, including dissolved organic carbon (DOC) and soil organic carbon (SOC). Results from a combination of laboratory and field experiments suggest that C decomposition in old, highly weathered oxisol soils is strongly constrained by P availability. In addition, P additions to these soils (no C added) also revealed that microbial utilization of at least labile fractions of SOC was also P limited. To our knowledge, this is the first direct evidence of P limitation of microbial processes in tropical rain forest soil. We suggest that P limitation of microbial decomposition may have profound implications for C cycling in moist tropical forests, including their potential response to increasing atmospheric carbon dioxide. Furthermore, this site is still relatively rich in P when compared to many other tropical forests on old soils; thus, we believe that P limitation of soil microorganisms throughout the humid tropics is a possibility.

Variations in the predicted spatial distribution of atmospheric nitrogen deposition and their impact on carbon uptake by terrestrial ecosystems

Widespread mobilization of nitrogen into the atmosphere from industry, agriculture, and biomass burning and its subsequent deposition have the potential to alleviate nitrogen limitation of productivity in terrestrial ecosystems, and may contribute to enhanced terrestrial carbon uptake. To evaluate the importance of the spatial distribution of nitrogen deposition for carbon uptake and to better quantify its magnitude and uncertainty NO y -N deposition fields from five different three-dimensional chemical models, GCTM, GRANTOUR, IMAGES, MOGUNTIA, and ECHAM were used to drive NDEP, a perturbation model of terrestrial carbon uptake. Differences in atmospheric sources of NO x -N, transport, resolution, and representation of chemistry, contribute to the distinct spatial patterns of nitrogen deposition on the global land surface; these differences lead to distinct patterns of carbon uptake that vary between 0.7 and 1.3 Gt C yr -1 globally. Less than 10% of the nitrogen was deposited on forests which were most able to respond with increased carbon storage because of the wide C:N ratio of wood as well as its long lifetime. Addition of NH x -N to NO y -N deposition, increased global terrestrial carbon storage to between 1.5 and 2.0 Gt C yr -1 , while the missing terrestrial sink is quite similar in magnitude. Thus global air pollution appears to be an important influence on the global carbon cycle. If N fertilization of the terrestrial biosphere accounts for the missing C sink or a substantial portion of it, we would expect significant reductions in its magnitude over the next century as terrestrial ecosystems become N saturated and O 3 pollution expands.

Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere

Terrestrial biosphere–atmosphere carbon dioxide (CO2) exchange is dominated by tropical forests, where photosynthetic carbon (C) uptake is thought to be phosphorus (P)-limited. In P-poor tropical forests, P may also limit organic matter decomposition and soil C losses. We conducted a field-fertilization experiment to show that P fertilization stimulates soil respiration in a lowland tropical rain forest in Costa Rica. In the early wet season, when soluble organic matter inputs to soil are high, P fertilization drove large increases in soil respiration. Although the P-stimulated increase in soil respiration was largely confined to the dry-to-wet season transition, the seasonal increase was sufficient to drive an 18% annual increase in CO2 efflux from the P-fertilized plots. Nitrogen (N) fertilization caused similar responses, and the net increases in soil respiration in response to the additions of N and P approached annual soil C fluxes in mid-latitude forests. Human activities are altering natural patterns of tropical soil N and P availability by land conversion and enhanced atmospheric deposition. Although our data suggest that the mechanisms driving the observed respiratory responses to increased N and P may be different, the large CO2 losses stimulated by N and P fertilization suggest that knowledge of such patterns and their effects on soil CO2 efflux is critical for understanding the role of tropical forests in a rapidly changing global C cycle.