Lars O. Hedin

Changing sources of nutrients during four million years of ecosystem development

As soils develop in humid environments, rock-derived elements are gradually lost, and under constant conditions it seems that ecosystems should reach a state of profound and irreversible nutrient depletion. We show here that inputs of elements from the atmosphere can sustain the productivity of Hawaiian rainforests on highly weathered soils. Cations are supplied in marine aerosols and phosphorus is deposited in dust from central Asia, which is over 6,000 km away.

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.

SCALING OF C:N:P STOICHIOMETRY IN FORESTS WORLDWIDE: IMPLICATIONS OF TERRESTRIAL REDFIELD-TYPE RATIOS

Inspired by the importance of globally well-constrained carbon:nitrogen: phosphorus (C:N:P) ratios in planktonic biomass to the understanding of nutrient cycles and biotic feedbacks in marine ecosystems, we looked for analogous patterns in forest ecosystems worldwide. We used data from the literature to examine the stoichiometry of C, N, and P in forest foliage and litter on both global and biome levels. Additionally, we examined the scaling of nutrient investments with biomass and production both globally and within biomes to determine if and when these ratios respond to macroscale ecosystem properties (such as nutrient availability). We found that, while global forest C:N:P ratios in both foliage and litter were more variable than those of marine particulate matter, biome level (temperate broadleaf, temperate coniferous, and tropical) ratios were as constrained as marine ratios and statistically distinct from one another. While we were more interested in the relative constancy of the C:N:P ratios than their numerical value we did note, as have others, that the atomic ratios calculated for foliage (1212:28:1) and litter (3007:45:1) reflect the increased proportion of C-rich structural material characteristic of terrestrial vegetation. Carbon : nutrient ratios in litter were consistently higher than in comparable foliar data sets, suggesting that resorption of nutrients is a globally important mechanism, particularly for P. Litter C:N ratios were globally constant despite biome-level differences in foliar C:N; we speculate that this strong coupling may be caused by the significant contribution of immobile cell wall bound proteins to the total foliar N pool. Most ratios scaled isometrically across the range of biomass stocks and production in all biomes sug- gesting that ratios arise directly from physiological constraints and are insensitive to factors leading to shifts in biomass and production. There were, however, important exceptions to this pattern: nutrient investment in broadleaf forest litter and coniferous forest foliage increased disproportionately relative to C with increasing biomass and production sug- gesting a systematic influence of macroscopic factors on ratios.

THERMODYNAMIC CONSTRAINTS ON NITROGEN TRANSFORMATIONS AND OTHER BIOGEOCHEMICAL PROCESSES AT SOIL-STREAM INTERFACES

There is much interest in biogeochemical processes that occur at the interface between soils and streams since, at the scale of landscapes, these habitats may function as control points for fluxes of nitrogen (N) and other nutrients from terrestrial to aquatic ecosystems. Here we examine whether a thermodynamic perspective can enhance our mechanistic and predictive understanding of the biogeochemical function of soil-stream interfaces, by considering how microbial communities interact with variations in supplies of electron donors and acceptors. Over a two-year period we analyzed >1400 individual samples of subsurface waters from networks of sample wells in riparian wetlands along Smith Creek, a first-order stream draining a mixed forested-agricultural landscape in southwestern Michigan, USA. We focused on areas where soil water and ground water emerged into the stream, and where we could characterize subsurface flow paths by measures of hydraulic head and/or by in situ additions of hydrologic tracers. We found strong support for the idea that the biogeochemical function of soil-stream interfaces is a predictable outcome of the interaction between microbial communities and supplies of electron donors and acceptors. Variations in key electron donors and acceptors (NO 3 - , N 2 O, NH 4 + , SO 4 2- , CH 4 , and dissolved organic carbon [DOC]) closely followed predictions from thermodynamic theory. Transformations of N and other elements resulted from the response of microbial communities to two dominant hydrologic flow paths: (1) horizontal flow of shallow subsurface waters with high levels of electron donors (i.e., DOC, CH 4 , and NH 4 + ), and (2) near-stream vertical upwelling of deep subsurface waters with high levels of energetically favorable electron acceptors (i.e., NO 3 - , N 2 O, and SO 4 2- ). Our results support the popular notion that soil-stream interfaces can possess strong potential for removing dissolved N by denitrification. Yet in contrast to prevailing ideas, we found that denitrification did not consume all NO 3 - that reached the soil-stream interface via subsurface flow paths. Analyses of subsurface N chemistry and natural abundances of δ 15 N in NO 3 - and NH 4 + suggested a narrow near-stream region as functionally the most important location for NO 3 - consumption by denitrification. This region was characterized by high throughput of terrestrially derived water, by accumulation of dissolved NO 3 - and N 2 O, and by low levels of DOC. Field experiments supported our hypothesis that the sustained ability for removal of dissolved NO 3 - and N 2 O should be limited by supplies of oxidizable carbon via shallow flowpaths. In situ additions of acetate, succinate, and propionate induced rates of NO 3 - removal (∼1.8 g N.m -2 .d -1 ) that were orders of magnitude greater than typically reported from riparian habitats. We propose that the immediate near-stream region may be especially important for determining the landscape-level function of many riparian wetlands. Management efforts to optimize the removal of NO 3 - by denitrification ought to consider promoting natural inputs of oxidizable carbon to this near-stream region.

THERMODYNAMIC CONSTRAINTS ON NITROGENTRANSFORMATIONS AND OTHER BIOGEOCHEMICALPROCESSES AT SOIL–STREAM INTERFACES

There is much interest in biogeochemical processes that occur at the interface between soils and streams since, at the scale of landscapes, these habitats may function as control points for fluxes of nitrogen (N) and other nutrients from terrestrial to aquatic ecosystems. Here we examine whether a thermodynamic perspective can enhance our mechanistic and predictive understanding of the biogeochemical function of soil–stream interfaces, by considering how microbial communities interact with variations in supplies of electron donors and acceptors. Over a two-year period we analyzed >1400 individual samples of subsurface waters from networks of sample wells in riparian wetlands along Smith Creek, a first-order stream draining a mixed forested–agricultural landscape in southwestern Michigan, USA. We focused on areas where soil water and ground water emerged into the stream, and where we could characterize subsurface flow paths by measures of hydraulic head and/or by in situ additions of hydrologic tracers. We found strong support for the idea that the biogeochemical function of soil–stream interfaces is a predictable outcome of the interaction between microbial communities and supplies of electron donors and acceptors. Variations in key electron donors and acceptors (NO3−, N2O, NH4+, SO42−, CH4, and dissolved organic carbon [DOC]) closely followed predictions from thermodynamic theory. Transformations of N and other elements resulted from the response of microbial communities to two dominant hydrologic flow paths: (1) horizontal flow of shallow subsurface waters with high levels of electron donors (i.e., DOC, CH4, and NH4+), and (2) near-stream vertical upwelling of deep subsurface waters with high levels of energetically favorable electron acceptors (i.e., NO3−, N2O, and SO42−). Our results support the popular notion that soil–stream interfaces can possess strong potential for removing dissolved N by denitrification. Yet in contrast to prevailing ideas, we found that denitrification did not consume all NO3− that reached the soil–stream interface via subsurface flow paths. Analyses of subsurface N chemistry and natural abundances of δ15N in NO3− and NH4+ suggested a narrow near-stream region as functionally the most important location for NO3− consumption by denitrification. This region was characterized by high throughput of terrestrially derived water, by accumulation of dissolved NO3− and N2O, and by low levels of DOC. Field experiments supported our hypothesis that the sustained ability for removal of dissolved NO3− and N2O should be limited by supplies of oxidizable carbon via shallow flowpaths. In situ additions of acetate, succinate, and propionate induced rates of NO3− removal (∼1.8 g N·m−2·d−1) that were orders of magnitude greater than typically reported from riparian habitats. We propose that the immediate near-stream region may be especially important for determining the landscape-level function of many riparian wetlands. Management efforts to optimize the removal of NO3− by denitrification ought to consider promoting natural inputs of oxidizable carbon to this near-stream region.

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest

We maintained a factorial nitrogen (N), phosphorus (P), and potassium (K) addition experiment for 11 years in a humid lowland forest growing on a relatively fertile soil in Panama to evaluate potential nutrient limitation of tree growth rates, fine-litter production, and fine-root biomass. We replicated the eight factorial treatments four times using 32 plots of 40 x 40 m each. The addition of K was associated with significant decreases in stand-level fine-root biomass and, in a companion study of seedlings, decreases in allocation to roots and increases in height growth rates. The addition of K and N together was associated with significant increases in growth rates of saplings and poles (1-10 cm in diameter at breast height) and a further marginally significant decrease in stand-level fine-root biomass. The addition of P was associated with a marginally significant (P = 0.058) increase in fine-litter production that was consistent across all litter fractions. Our experiment provides evidence that N, P, and K all limit forest plants growing on a relatively fertile soil in the lowland tropics, with the strongest evidence for limitation by K among seedlings, saplings, and poles.

NUTRIENT LOSSES OVER FOUR MILLION YEARS OF TROPICAL FOREST DEVELOPMENT

Biological, atmospheric, and geochemical processes interact to shape how element cycles and nutrient losses develop within newly formed landscapes. We examined losses of nitrogen (N), phosphorus (P), and base cations across a four-million-year substrate age gradient of Hawaiian montane tropical forests, with the goal of understanding how losses depend on changes in biotic demand, weathering, and atmospheric sources. We were particularly interested in whether losses of nutrients that are not subject to traditional mechanisms of biotic availability could influence ecosystem fertility and nutrient limitation over time. Over a three-year period we sampled nutrient outputs in soil solutions below the active plant-soil system and small streams, gaseous N losses (NO, N2O, and N2), and pools and transformations of N in soils. Weathering was the major determinant of ecosystem losses of P, of base cations and Si, and of ecosystem acid-base status. Sharp reductions in weathering inputs after 20 000 years of forest development caused dramatically lower outputs of P (;65% reduction), Ca 2 1 (;99%), and Si (;94%), to rates that matched inputs from dilute sea-salt and dust aerosols. Internal production of organic acids, in combination with low weathering, caused highly acidic soil waters (pH , 5.0) with elevated Al (up to 300 mg/L) and Ca:Al ratios (,0.3) below values considered critical thresholds for many plant species. Long-term N and P interactions were more complex than predicted by the Walker and Syers model, with important influences of N and P loss pathways that were not subject to direct biotic availability. While losses of available forms of dissolved N and P, and N gases followed (as predicted) ecosystem nutrient availability, significant dissolved organic N (DON) and dissolved organic P (DOP) losses occurred independent of ecosystem N or P status. DON losses were not sufficient (relative to external inputs) to sustain N limitation beyond 20 000 years, while dissolved P losses remained large enough to maintain P lim- itation in older forests. Forests developed high N:P loss ratios over time ( .300 on mass weight basis) due to efficient P recycling and unexpectedly high N throughputs (4-9 kg N·ha 21 ·yr 21 ) by either N fixation and/or N deposition.

Key role of symbiotic dinitrogen fixation in tropical forest secondary succession

Forests contribute a significant portion of the land carbon sink, but their ability to sequester CO2 may be constrained by nitrogen, a major plant-limiting nutrient. Many tropical forests possess tree species capable of fixing atmospheric dinitrogen (N2), but it is unclear whether this functional group can supply the nitrogen needed as forests recover from disturbance or previous land use, or expand in response to rising CO2 (refs 6, 8). Here we identify a powerful feedback mechanism in which N2 fixation can overcome ecosystem-scale deficiencies in nitrogen that emerge during periods of rapid biomass accumulation in tropical forests. Over a 300-year chronosequence in Panama, N2-fixing tree species accumulated carbon up to nine times faster per individual than their non-fixing neighbours (greatest difference in youngest forests), and showed species-specific differences in the amount and timing of fixation. As a result of fast growth and high fixation, fixers provided a large fraction of the nitrogen needed to support net forest growth (50,000 kg carbon per hectare) in the first 12 years. A key element of ecosystem functional diversity was ensured by the presence of different N2-fixing tree species across the entire forest age sequence. These findings show that symbiotic N2 fixation can have a central role in nitrogen cycling during tropical forest stand development, with potentially important implications for the ability of tropical forests to sequester CO2.

Within-System Element Cycles, Input-Output Budgets, and Nutrient Limitation

Widely used conceptual models for controls on nutrient cycling and input-outputs budgets of forest ecosystems suggest that: (1) nutrient losses from ecosystems originate in the available nutrient pool in soil; (2) nutrients that limit plant production are retained tightly within those systems; (3) this retention leads to accumulation of the limiting nutrient(s), eventually to the point at which it no longer limits production; and (4) losses of nutrient(s) thereafter should reflect rates of nutrient input, rather than biotic demand In this chapter, we explore mechanisms that could constrain the accumulation of a limiting nutrient, and therefore could allow nutrient limitation to persist indefinitely. Possible mechanisms include episodic disturbance-related nutrient losses, closed element cycles, and losses of nutrients from sources other than the available inorganic pool of nutrients in soil. For the last mechanism, both a simple and a more complex model are used to show that losses of dissolved organic forms of a nutrient could constrain nutrient accumulation and permit nutrient limitation to persist indefintely. Emissions of nitrogen (N) trace gases produced during nitrification could have a similar effect. To the extent that losses of nutrients by these and related pathways are important, anthropogenic inputs of nutrients (particularly N) could alter forest ecosystems substantially, to an extent greater than standard conceptual models would allow.

Complex response of the forest nitrogen cycle to climate change

Climate exerts a powerful influence on biological processes, but the effects of climate change on ecosystem nutrient flux and cycling are poorly resolved. Although rare, long-term records offer a unique opportunity to disentangle effects of climate from other anthropogenic influences. Here, we examine the longest and most complete record of watershed nutrient and climate dynamics available worldwide, which was collected at the Hubbard Brook Experimental Forest in the northeastern United States. We used empirical analyses and model calculations to distinguish between effects of climate change and past perturbations on the forest nitrogen (N) cycle. We find that climate alone cannot explain the occurrence of a dramatic >90% drop in watershed nitrate export over the past 46 y, despite longer growing seasons and higher soil temperatures. The strongest climate influence was an increase in soil temperature accompanied by a shift in paths of soil water flow within the watershed, but this effect explained, at best, only ∼40% of the nitrate decline. In contrast, at least 50–60% of the observed change in the N export could be explained by the long-lasting effect of forest cutting in the early 1900s on the N cycle of the soil and vegetation pools. Our analysis shows that historic events can obscure the influence of modern day stresses on the N cycle, even when analyses have the advantage of being informed by 0.5-century-long datasets. These findings raise fundamental questions about interpretations of long-term trends as a baseline for understanding how climate change influences complex ecosystems.