Donald R. Zak

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.

Plant diversity, soil microbial communities, and ecosystem function: Are there any links?

A current debate in ecology centers on the extent to which ecosystem function depends on biodiversity. Here, we provide evidence from a long-term field manipulation of plant diversity that soil microbial communities, and the key ecosystem processes that they mediate, are significantly altered by plant species richness. After seven years of plant growth, we determined the composition and function of soil microbial communities beneath experimental plant diversity treatments containing 1-16 species. Microbial community bio- mass, respiration, and fungal abundance significantly increased with greater plant diversity, as did N mineralization rates. However, changes in microbial community biomass, activity, and composition largely resulted from the higher levels of plant production associated with greater diversity, rather than from plant diversity per se. Nonetheless, greater plant pro- duction could not explain more rapid N mineralization, indicating that plant diversity affected this microbial process, which controls rates of ecosystem N cycling. Greater N availability probably contributed to the positive relationship between plant diversity and productivity in the N-limited soils of our experiment, suggesting that plant-microbe in- teractions in soil are an integral component of plant diversitys influence on ecosystem

Stoichiometry of soil enzyme activity at global scale

Extracellular enzymes are the proximate agents of organic matter decomposition and measures of these activities can be used as indicators of microbial nutrient demand. We conducted a global-scale meta-analysis of the seven-most widely measured soil enzyme activities, using data from 40 ecosystems. The activities of beta-1,4-glucosidase, cellobiohydrolase, beta-1,4-N-acetylglucosaminidase and phosphatase g(-1) soil increased with organic matter concentration; leucine aminopeptidase, phenol oxidase and peroxidase activities showed no relationship. All activities were significantly related to soil pH. Specific activities, i.e. activity g(-1) soil organic matter, also varied in relation to soil pH for all enzymes. Relationships with mean annual temperature (MAT) and precipitation (MAP) were generally weak. For hydrolases, ratios of specific C, N and P acquisition activities converged on 1 : 1 : 1 but across ecosystems, the ratio of C : P acquisition was inversely related to MAP and MAT while the ratio of C : N acquisition increased with MAP. Oxidative activities were more variable than hydrolytic activities and increased with soil pH. Our analyses indicate that the enzymatic potential for hydrolyzing the labile components of soil organic matter is tied to substrate availability, soil pH and the stoichiometry of microbial nutrient demand. The enzymatic potential for oxidizing the recalcitrant fractions of soil organic material, which is a proximate control on soil organic matter accumulation, is most strongly related to soil pH. These trends provide insight into the biogeochemical processes that create global patterns in ecological stoichiometry and organic matter storage.

The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil

Anthropogenic N deposition affects litter decomposition and soil organic matter (SOM) storage through multiple mechanisms. Microbial community responses to long-term N deposition were investigated in a sugar maple-dominated forest in northern Michigan during the 1998– 2000 growing seasons. Litter and soil were collected from three fertilized plots (30 kg N ha 21 y 21 ) and three control plots. The activities of 10 extracellular enzymes (EEA) were assayed. ANOVA and meta-analysis techniques were used to compare treatment responses. EEA responses to N amendment were greater in litter than in soil (litter mean effect size [d ] ¼ 0.534 std. dev.; soil d ¼ 0:308). Urease, acid phosphatase and glycosidase (b-glucosidase, a-glucosidase, cellobiohydrolase, b-xylosidase) activities increased in both soil and litter; mean responses ranged from 7 to 56%. N-Acetylglucosaminidase activity increased 14% in soil but decreased 4% in litter. Phenol oxidase activity dropped 40% in soil, but increased 63% in litter. These responses suggest that N deposition has increased litter decomposition rate and depressed SOM decomposition. In previous studies, loss of phenol oxidase activity in response to N deposition has been attributed to suppression of lignin-degrading basidiomycetes. However, the decline of this activity in bacterially-dominated soil suggest that N inhibition of recalcitrant organic matter decomposition may be a more general phenomenon. q 2002 Elsevier Science Ltd. All rights reserved.

Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles

We tested a conceptual model describing the influence of elevated atmospheric CO2 on plant production, soil microorganisms, and the cycling of C and N in the plant-soil system. Our model is based on the observation that in nutrient-poor soils, plants (C3) grown in an elevated CO2 atmosphere often increase production and allocation to belowground structures. We predicted that greater belowground C inputs at elevated CO2 should elicit an increase in soil microbial biomass and increased rates of organic matter turnover and nitrogen availability. We measured photosynthesis, biomass production, and C allocation of Populus grandidentata Michx. grown in nutrient-poor soil for one field season at ambient and twice-ambient (i.e., elevated) atmospheric CO2 concentrations. Plants were grown in a sandy subsurface soil i) at ambient CO2 with no open top chamber, ii) at ambient CO2 in an open top chamber, and iii) at twice-ambient CO2 in an open top chamber. Plants were fertilized with 4.5 g N m−2 over a 47 d period midway through the growing season. Following 152 d of growth, we quantified microbial biomass and the availabilities of C and N in rhizosphere and bulk soil. We tested for a significant CO2 effect on plant growth and soil C and N dynamics by comparing the means of the chambered ambient and chambered elevated CO2 treatments.Rates of photosynthesis in plants grown at elevated CO2 were significantly greater than those measured under ambient conditions. The number of roots, root length, and root length increment were also substantially greater at elevated CO2. Total and belowground biomass were significantly greater at elevated CO2. Under N-limited conditions, plants allocated 50–70% of their biomass to roots. Labile C in the rhizosphere of elevated-grown plants was significantly greater than that measured in the ambient treatments; there were no significant differences between labile C pools in the bulk soil of ambient and elevated-grown plants. Microbial biomass C was significantly greater in the rhizosphere and bulk soil of plants grown at elevated CO2 compared to that in the ambient treatment. Moreover, a short-term laboratory assay of N mineralization indicated that N availability was significantly greater in the bulk soil of the elevated-grown plants. Our results suggest that elevated atmospheric CO2 concentrations can have a positive feedback effect on soil C and N dynamics producing greater N availability. Experiments conducted for longer periods of time will be necessary to test the potential for negative feedback due to altered leaf litter chemistry. ei]{gnH}{fnLambers} ei]{gnA C}{fnBorstlap}

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.

Nitrogen Deposition Modifies Soil Carbon Storage Through Changes In Microbial Enzymatic Activity

Atmospheric nitrogen (N) deposition derived from fossil-fuel combustion, land clearing, and biomass burning is occurring over large geographical regions on nearly every continent. Greater ecosystem N availability can result in greater aboveground carbon (C) sequestration, but little is understood as to how soil C storage could be altered by N deposition. High concentrations of inorganic N accelerate the degradation of easily decom- posable litter and slow the decomposition of recalcitrant litter containing large amounts of lignin. This pattern has been attributed to stimulation or repression of different sets of microbial extracellular enzymes. We hypothesized that soil C cycling in forest ecosystems with markedly different litter chemistry and decomposition rates would respond to anthro- pogenic N deposition in a manner consistent with the biochemical composition of the dominant vegetation. Specifically, oak-dominated ecosystems with low litter quality should gain soil C, and sugar maple ecosystems with high litter quality should lose soil C in response to high levels of N deposition (80 kg N-ha-1-yr-1). Consistent with this hypothesis, we observed over a three-year period a significant loss of soil C (20%) from a sugar maple- dominated ecosystem and a significant gain (10%) in soil C in an oak-dominated ecosystem, a result that appears to be mediated by the regulation of the microbial extracellular enzyme phenol oxidase. Elevated N deposition resulted in changes in soil carbon that were ecosystem specific and resulted from the divergent regulatory control of microbial extracellular en- zymes by soil N availability.

THE VERNAL DAM: PLANT-MICROBE COMPETITION FOR NITROGEN IN NORTHERN HARDWOOD FORESTS'

Nitrogen (N) uptake by spring ephemeral communities has been proposed as a mechanism that retains N within northern hardwood forests during the season of maximum loss. To understand better the importance of these plants in retaining N, we followed the movement of 15NH4+ and 15N03- into plant and microbial biomass. Two days following isotope addition, microbial biomass represented the largest labile pool of N and contained 8.5 times as much N as Allium tricoccum L. biomass. Microbial immobilization of 15N was 10-20 times greater than uptake by A. tricoccum. Nitrification of 15NH4, was five times lower in cores containing A. tricoccum compared to those without the spring ephemeral. Spring N retention within northern hardwood forests cannot be fully explained by plant uptake because microbial immobilization represented a significantly larger sink for N. Results suggest that plant and microbial uptake of NH4, may reduce the quantity of substrate available for nitrification and thereby lessen the potential for N03- loss via denitrification and leaching.

Altered performance of forest pests under atmospheres enriched by CO2 and O3

Human activity causes increasing background concentrations of the greenhouse gases CO2 and O3. Increased levels of CO2 can be found in all terrestrial ecosystems. Damaging O3 concentrations currently occur over 29% of the worlds temperate and subpolar forests but are predicted to affect fully 60% by 2100 (ref. 3). Although individual effects of CO2 and O3 on vegetation have been widely investigated, very little is known about their interaction, and long-term studies on mature trees and higher trophic levels are extremely rare. Here we present evidence from the most widely distributed North American tree species, Populus tremuloides, showing that CO2 and O3, singly and in combination, affected productivity, physical and chemical leaf defences and, because of changes in plant quality, insect and disease populations. Our data show that feedbacks to plant growth from changes induced by CO2 and O3 in plant quality and pest performance are likely. Assessments of global change effects on forest ecosystems must therefore consider the interacting effects of CO2 and O3 on plant performance, as well as the implications of increased pest activity.

Dynamics of vesicular-arbuscular mycorrhizae during old field succession

SummaryThe species composition of vesicular-arbuscular mycorrhizal (VAM) fungal communities changed during secondary succession of abandoned fields based on a field to forest chronosequence. Twenty-five VAM fungal species were identified. Seven species were clearly early successional and five species were clearly late successional. The total number of VAM fungal species did not increase with successional time, but diversity as measured by the Shannon-Wiener index tended to increase, primarily because the community became more even as a single species, Glomus aggregatum, became less dominant in the older sites. Diversity of the VAM fungal community was positively correlated with soil C and N. The density of VAM fungi, as measured by infectivity and total spore count, first increased with time since abandonment and then decreased in the late successional forest sites. Within 12 abandoned fields, VAM fungal density increased with increasing soil pH, H2O soluble soil C, and root biomass, but was inversely related to extractable soil P and percent cover of non-host plant species. The lower abundance of VAM fungi in the forest sites compared with the field sites agrees with the findings of other workers and corresponds with a shift in the dominant vegetation from herbaceous VAM hosts to woody ectomycorrhizal hosts.