Adrien C. Finzi

Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide

Abstract A highly controversial issue in global biogeochemistry is the regulation of terrestrial carbon (C) sequestration by soil nitrogen (N) availability. This controversy translates into great uncertainty in predicting future global terrestrial C sequestration. We propose a new framework that centers on the concept of progressive N limitation (PNL) for studying the interactions between C and N in terrestrial ecosystems. In PNL, available soil N becomes increasingly limiting as C and N are sequestered in long-lived plant biomass and soil organic matter. Our analysis focuses on the role of PNL in regulating ecosystem responses to rising atmospheric carbon dioxide concentration, but the concept applies to any perturbation that initially causes C and N to accumulate in organic forms. This article examines conditions under which PNL may or may not constrain net primary production and C sequestration in terrestrial ecosystems. While the PNL-centered framework has the potential to explain diverse experimental results and to help researchers integrate models and data, direct tests of the PNL hypothesis remain a great challenge to the research community.

CANOPY TREE–SOIL INTERACTIONS WITHIN TEMPERATE FORESTS: SPECIES EFFECTS ON SOIL CARBON AND NITROGEN

In a northwestern Connecticut forest, we quantified the carbon (C) and ni- trogen (N) content of the forest floor and the top 15 cm of mineral soil and the rate of midsummer net N mineralization beneath six different tree species. There were large in- terspecific differences in forest floor depth and mass, in the size and distribution of C and N pools at varying soil depths, and in rates of midsummer net N mineralization and nitri- fication. Forest floor mass ranged from 3.2 kg/m 2 to 11.0 kg/m 2 and was smallest beneath sugar maple and largest beneath hemlock. The pool size of C in the forest floor ranged from 1.1 kg/m 2 to 4.4 kg/m 2 while the N content of the forest floor ranged from 83 g/m 2 to 229 g/m 2 . Forest floor C and N pools were smallest beneath sugar maple and highest beneath hemlock. Soil C:N ratios (range: 14.8-19.5) were lower beneath sugar maple, red maple, and white ash than beneath beech, red oak, and hemlock, whereas the opposite was true of the midsummer rate of net N mineralization (range: 0.91-2.02 g·m 22 ·28 d 21 ). The rate of net nitrification was positively correlated with the rate of net N mineralization. Interspecific differences in litter production and quality explain the large differences among species in the size of the forest floor C and N pools and in net N mineralization rates. The differences in the size and distribution of C and N pools beneath the different species suggest that the mechanisms regulating the process of species replacement in these forests will mediate the effects of anthropogenic, environmental changes in soil C and N dynamics.

CANOPY TREE-SOIL INTERACTIONS WITHIN TEMPERATE FORESTS: SPECIES EFFECTS ON pH AND CATIONS

We quantified soil acidity and exchangeable cations in the forest floor and upper 7.5 cm of mineral soil beneath the canopies of individual trees of six different species in a mixed-species forest in northwestern Connecticut. Soil pH decreased in a sequence starting with sugar maple (Acer saccharum) . white ash (Fraxinus americana) . red maple (Acer rubrum) . beech (Fagus grandifolia) . red oak (Quercus rubra) . eastern hemlock (Tsuga canadensis). The differences among species were largest in the forest floor and the top 7.5 cm of mineral soil. Exchangeable Ca and Mg in the 0-7.5 cm mineral soil layer were significantly higher beneath sugar maple than all other species, with the exception of white ash. There were negligible differences among species in the quantity of exchangeable Ca and Mg in the forest floor. In the 0-7.5 cm mineral soil layer, exchangeable Ca was positively correlated with the content of unweathered Ca in the parent material, but the relationship differed among species. There was a large increase in exchangeable Ca in the soils beneath sugar maple but a negligible increase in the soils beneath hemlock and red maple. Exchangeable Al and Fe were highest beneath hemlock and lowest beneath sugar maple. The differences in pH and exchangeable cations between sugar maple and hemlock are likely due to interspecific differences in the introduction of acidity (e.g., organic acids) and Ca uptake and allocation. Observing an association between tree species and specific soil chemical properties within mixed-species stands implies that changes in the distribution and abundance of tree species alters the spatial and temporal pattern of soil acidity and cation cycling in this forest.

Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation

The degree to which rising atmospheric CO(2) will be offset by carbon (C) sequestration in forests depends in part on the capacity of trees and soil microbes to make physiological adjustments that can alleviate resource limitation. Here, we show for the first time that mature trees exposed to CO(2) enrichment increase the release of soluble C from roots to soil, and that such increases are coupled to the accelerated turnover of nitrogen (N) pools in the rhizosphere. Over the course of 3 years, we measured in situ rates of root exudation from 420 intact loblolly pine (Pinus taeda L.) roots. Trees fumigated with elevated CO(2) (200 p.p.m.v. over background) increased exudation rates (μg C cm(-1) root h(-1) ) by 55% during the primary growing season, leading to a 50% annual increase in dissolved organic inputs to fumigated forest soils. These increases in root-derived C were positively correlated with microbial release of extracellular enzymes involved in breakdown of organic N (R(2) = 0.66; P = 0.006) in the rhizosphere, indicating that exudation stimulated microbial activity and accelerated the rate of soil organic matter (SOM) turnover. In support of this conclusion, trees exposed to both elevated CO(2) and N fertilization did not increase exudation rates and had reduced enzyme activities in the rhizosphere. Collectively, our results provide field-based empirical support suggesting that sustained growth responses of forests to elevated CO(2) in low fertility soils are maintained by enhanced rates of microbial activity and N cycling fuelled by inputs of root-derived C. To the extent that increases in exudation also stimulate SOM decomposition, such changes may prevent soil C accumulation in forest ecosystems.

Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage

Soil contains more carbon than the atmosphere and vegetation combined. Understanding the mechanisms controlling the accumulation and stability of soil carbon is critical to predicting the Earth’s future climate. Recent studies suggest that decomposition of soil organic matter is often limited by nitrogen availability to microbes and that plants, via their fungal symbionts, compete directly with free-living decomposers for nitrogen. Ectomycorrhizal and ericoid mycorrhizal (EEM) fungi produce nitrogen-degrading enzymes, allowing them greater access to organic nitrogen sources than arbuscular mycorrhizal (AM) fungi. This leads to the theoretical prediction that soil carbon storage is greater in ecosystems dominated by EEM fungi than in those dominated by AM fungi. Using global data sets, we show that soil in ecosystems dominated by EEM-associated plants contains 70% more carbon per unit nitrogen than soil in ecosystems dominated by AM-associated plants. The effect of mycorrhizal type on soil carbon is independent of, and of far larger consequence than, the effects of net primary production, temperature, precipitation and soil clay content. Hence the effect of mycorrhizal type on soil carbon content holds at the global scale. This finding links the functional traits of mycorrhizal fungi to carbon storage at ecosystem-to-global scales, suggesting that plant–decomposer competition for nutrients exerts a fundamental control over the terrestrial carbon cycle.

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

Forest ecosystems are important sinks for rising concentrations of atmospheric CO2. In previous research, we showed that net primary production (NPP) increased by 23 ± 2% when four experimental forests were grown under atmospheric concentrations of CO2 predicted for the latter half of this century. Because nitrogen (N) availability commonly limits forest productivity, some combination of increased N uptake from the soil and more efficient use of the N already assimilated by trees is necessary to sustain the high rates of forest NPP under free-air CO2 enrichment (FACE). In this study, experimental evidence demonstrates that the uptake of N increased under elevated CO2 at the Rhinelander, Duke, and Oak Ridge National Laboratory FACE sites, yet fertilization studies at the Duke and Oak Ridge National Laboratory FACE sites showed that tree growth and forest NPP were strongly limited by N availability. By contrast, nitrogen-use efficiency increased under elevated CO2 at the POP-EUROFACE site, where fertilization studies showed that N was not limiting to tree growth. Some combination of increasing fine root production, increased rates of soil organic matter decomposition, and increased allocation of carbon (C) to mycorrhizal fungi is likely to account for greater N uptake under elevated CO2. Regardless of the specific mechanism, this analysis shows that the larger quantities of C entering the below-ground system under elevated CO2 result in greater N uptake, even in N-limited ecosystems. Biogeochemical models must be reformulated to allow C transfers below ground that result in additional N uptake under elevated CO2.

Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2

The earths future climate state is highly dependent upon changes in terrestrial C storage in response to rising concentrations of atmospheric CO₂. Here we show that consistently enhanced rates of net primary production (NPP) are sustained by a C-cascade through the root-microbe-soil system; increases in the flux of C belowground under elevated CO₂ stimulated microbial activity, accelerated the rate of soil organic matter decomposition and stimulated tree uptake of N bound to this SOM. This process set into motion a positive feedback maintaining greater C gain under elevated CO₂ as a result of increases in canopy N content and higher photosynthetic N-use efficiency. The ecosystem-level consequence of the enhanced requirement for N and the exchange of plant C for N belowground is the dominance of C storage in tree biomass but the preclusion of a large C sink in the soil.

FOREST LITTER PRODUCTION, CHEMISTRY, AND DECOMPOSITION FOLLOWING TWO YEARS OF FREE-AIR CO2 ENRICHMENT

Increases in tree biomass may be an important sink for CO 2 as the atmospheric concentration continues to increase. Tree growth in temperate forests is often limited by the availability of soil nutrients. To assess whether soil nutrient limitation will constrain forest productivity under high atmospheric CO 2 , we studied the changes in forest litter production and nutrient cycling in a maturing southern U.S. loblolly pine–hardwood forest during two years of free-air CO 2 enrichment. The objective of this paper is to present data on the chemistry of green leaves and leaf litter, nutrient-retranslocation efficiency, aboveground litter production, whole-system nutrient-use efficiency, decomposition, and N availability in response to forest growth under elevated CO 2 . The chemical composition of green leaves and leaf litter was largely unaffected by elevated CO 2 . Green-leaf nitrogen (N) and phosphorus (P) concentrations were not significantly lower under elevated CO 2 . N and P retranslocation from green leaves did not increase under elevated CO 2 ; therefore, leaf litter N and P concentrations were not significantly lower under elevated CO 2 . The concentrations of carbon, lignin, and total nonstructural carbohydrates in litter were not significantly different under elevated CO 2 . Total aboveground litterfall increased significantly with CO 2 fumigation. The increase in litterfall was due to significant increases in loblolly pine leaf litter and bark production. The mass of leaves from deciduous species did not increase with CO 2 fumigation. Whole-system nutrient-use efficiency (aboveground litterfall/nutrient content of litterfall) did not increase as a consequence of forest growth under elevated CO 2 , but N and P fluxes from vegetation to the forest floor increased significantly. During the second year of CO 2 fumigation, the flux of N and P to the forest floor in litterfall increased by 20% and 34%, respectively. The rate of mass loss during one year of decomposition was unaffected by “litter type” (whether the litter was produced under ambient or elevated CO 2 ), nor by the “site” of decomposition (whether the litter was decomposed in the ambient or elevated CO 2 plots). N was immobilized in litter during decomposition, whereas P was mineralized. There was no consistent effect of litter type or site on nutrient dynamics in decomposing litter. There was no significant effect of elevated CO 2 on the pool size of inorganic N (NH 4 + and NO 3 − ) in the top 7.5 cm of mineral soil. The rate of net N mineralization and nitrification in mineral soil was not significantly different between treatment and control plots. Identifying the source of the nutrients lost in litterfall is critical to the long-term potential growth stimulation of forests under elevated CO 2 . If the nutrients lost from biomass come from storage (e.g., the movement of nutrients from wood to leaves), then the increase in litter production should decrease over time as slowly replenished nutrient reserves are exhausted. If the nutrients lost in plant litter are replaced by uptake from soils, then it is possible (1) that trees acquire soil nutrients at a rate commensurate with growth stimulated by elevated CO 2 ; and (2) that forest productivity will be stimulated by elevated CO 2 in the long term.

Re‐assessment of plant carbon dynamics at the Duke free‐air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development

*The potential for elevated [CO(2)]-induced changes to plant carbon (C) storage, through modifications in plant production and allocation of C among plant pools, is an important source of uncertainty when predicting future forest function. Utilizing 10 yr of data from the Duke free-air CO(2) enrichment site, we evaluated the dynamics and distribution of plant C. *Discrepancy between heights measured for this study and previously calculated heights required revision of earlier allometrically based biomass determinations, resulting in higher (up to 50%) estimates of standing biomass and net primary productivity than previous assessments. *Generally, elevated [CO(2)] caused sustained increases in plant biomass production and in standing C, but did not affect the partitioning of C among plant biomass pools. Spatial variation in net primary productivity and its [CO(2)]-induced enhancement was controlled primarily by N availability, with the difference between precipitation and potential evapotranspiration explaining most interannual variability. Consequently, [CO(2)]-induced net primary productivity enhancement ranged from 22 to 30% in different plots and years. *Through quantifying the effects of nutrient and water availability on the forest productivity response to elevated [CO(2)], we show that net primary productivity enhancement by elevated [CO(2)] is not uniform, but rather highly dependent on the availability of other growth resources.

Plant-soil interactions: ecological aspects and evolutionary implications.

Building on the concept of plants as ecosystem engineers, and on published information on effects of particular plant species on soils, we review the evidence that such effects can provide a positive feedback to such plants. Based on case studies involving dune formation by Marram grass, N supply by N2-fixing plants, depression of N availability by ericaceous plants, ‘islands of fertility’ in deserts, mull- and mor-forming temperate forest trees, and formation of peatbogs, as well as similar other cases, we conclude that there is strong evidence for plant-soil feedbacks in a variety of ecosystems. We argue, moreover, that these feedbacks could have played a role in the evolution of the plant species in question. These ideas are based mainly on correlative observations, and need further testing.