Richard J. Norby

Elevated CO2, litter chemistry, and decomposition: a synthesis

The results of published and unpublished experiments investigating the impacts of elevated [CO2] on the chemistry of leaf litter and decomposition of plant tissues are summarized. The data do not support the hypothesis that changes in leaf litter chemistry often associated with growing plants under elevated [CO2] have an impact on decomposition processes. A meta-analysis of data from naturally senesced leaves in field experiments showed that the nitrogen (N) concentration in leaf litter was 7.1% lower in elevated [CO2] compared to that in ambient [CO2]. This statistically significant difference was: (1) usually not significant in individual experiments, (2) much less than that often observed in green leaves, and (3) less in leaves with an N concentration indicative of complete N resorption. Under ideal conditions, the efficiency with which N is resorbed during leaf senescence was found not to be altered by CO2 enrichment, but other environmental influences on resorption inevitably increase the variability in litter N concentration. Nevertheless, the small but consistent decline in leaf litter N concentration in many experiments, coupled with a 6.5% increase in lignin concentration, would be predicted to result in a slower decomposition rate in CO2-enriched litter. However, across the assembled data base, neither mass loss nor respiration rates from litter produced in elevated [CO2] showed any consistent pattern or differences from litter grown in ambient [CO2]. The effects of [CO2] on litter chemistry or decomposition were usually smallest under experimental conditions similar to natural field conditions, including open-field exposure, plants free-rooted in the ground, and complete senescence. It is concluded that any changes in decomposition rates resulting from exposure of plants to elevated [CO2] are small when compared to other potential impacts of elevated [CO2] on carbon and N cycling. Reasons for experimental differences are considered, and recommendations for the design and execution of decomposition experiments using materials from CO2-enrichment experiments are outlined.

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.

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes.

Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally - a c. 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.

NET PRIMARY PRODUCTIVITY OF A CO2‐ENRICHED DECIDUOUS FOREST AND THE IMPLICATIONS FOR CARBON STORAGE

A central question concerning the response of terrestrial ecosystems to a changing atmosphere is whether increased uptake of carbon in response to increasing at- mospheric carbon dioxide concentration results in greater plant biomass and carbon storage or, alternatively, faster cycling of C through the ecosystem. Net primary productivity (NPP) of a closed-canopy Liquidambar styraciflua (sweetgum) forest stand was assessed for three years in a free-air CO2-enrichment (FACE) experiment. NPP increased 21% in stands ex- posed to elevated CO2, and there was no loss of response over time. Wood increment increased significantly during the first year of exposure, but subsequently most of the extra C was allocated to production of leaves and fine roots. These pools turn over more rapidly than wood, thereby reducing the potential of the forest stand to sequester additional C in response to atmospheric CO2 enrichment. Hence, while this experiment provides the first evidence that CO2 enrichment can increase productivity in a closed-canopy deciduous forest, the implications of this result must be tempered because the increase in productivity resulted in faster cycling of C through the system rather than increased C storage in wood. The fate of the additional C entering the soil system and the environmental interactions that influence allocation need further investigation.

Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide

A thorough assessment of how plants and ecosystems will respond to increasing concentrations of atmospheric CO2 requires that the responses of root systems and associated belowground processes be understood. Static measures of root-to-shoot ratio have not been satisfactory for describing the integrated responses of plants to CO2-enriched atmospheres, but research with a process orientation has suggested that elevated CO2 can stimulate root growth or root activity and provide a positive feedback on plant growth. There are, however, critical questions concerning the relevance of root data from short-term studies with potted plants when scaling to questions about plants in the field. Data on root responses to CO2 enrichment in the field are fragmentary, but they allow us to more clearly define research questions for further investigation. Three perspectives for analyzing the significance of root responses as a component of the overall response of the terrestrial biosphere to increasing atmospheric CO2 are suggested: (1) roots as a platform for nutrient acquisition and a mediator of whole-plant response to CO2; (2) carbon storage in roots as a component of whole-plant carbon storage; and (3) effects of CO2 enrichment on root turnover and the implications for carbon storage as soil organic matter. The relative importance of these different perspectives will vary depending on the ecosystem of interest and the larger-scale issues being considered.

Sensitivity of plants to changing atmospheric CO2 concentration : from the geological past to the next century

The rate of CO(2) assimilation by plants is directly influenced by the concentration of CO(2) in the atmosphere, c(a). As an environmental variable, c(a) also has a unique global and historic significance. Although relatively stable and uniform in the short term, global c(a) has varied substantially on the timescale of thousands to millions of years, and currently is increasing at seemingly an unprecedented rate. This may exert profound impacts on both climate and plant function. Here we utilise extensive datasets and models to develop an integrated, multi-scale assessment of the impact of changing c(a) on plant carbon dioxide uptake and water use. We find that, overall, the sensitivity of plants to rising or falling c(a) is qualitatively similar across all scales considered. It is characterised by an adaptive feedback response that tends to maintain 1 - c(i)/c(a), the relative gradient for CO(2) diffusion into the leaf, relatively constant. This is achieved through predictable adjustments to stomatal anatomy and chloroplast biochemistry. Importantly, the long-term response to changing c(a) can be described by simple equations rooted in the formulation of more commonly studied short-term responses.

Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate Free-Air CO2 Enrichment studies

We analysed the responses of 11 ecosystem models to elevated atmospheric [CO2] (eCO2) at two temperate forest ecosystems (Duke and Oak Ridge National Laboratory (ORNL) Free-Air CO2 Enrichment (FACE) experiments) to test alternative representations of carbon (C)–nitrogen (N) cycle processes. We decomposed the model responses into component processes affecting the response to eCO2 and confronted these with observations from the FACE experiments. Most of the models reproduced the observed initial enhancement of net primary production (NPP) at both sites, but none was able to simulate both the sustained 10-yr enhancement at Duke and the declining response at ORNL: models generally showed signs of progressive N limitation as a result of lower than observed plant N uptake. Nonetheless, many models showed qualitative agreement with observed component processes. The results suggest that improved representation of above-ground–below-ground interactions and better constraints on plant stoichiometry are important for a predictive understanding of eCO2 effects. Improved accuracy of soil organic matter inventories is pivotal to reduce uncertainty in the observed C–N budgets. The two FACE experiments are insufficient to fully constrain terrestrial responses to eCO2, given the complexity of factors leading to the observed diverging trends, and the consequential inability of the models to explain these trends. Nevertheless, the ecosystem models were able to capture important features of the experiments, lending some support to their projections.

A question of litter quality

One aspect of how terrestrial ecosystems will respond to rising levels of CO2in the atmosphere is potential changes in the decomposition rate of leaf litter - a central factor in plant growth. It had been thought that the decomposition rate would decline in high CO2conditions, but this long-established hypothesis was laid to rest at a meeting in September of plant physiologists, ecologists and soil scientists.

SOIL NITROGEN CYCLING UNDER ELEVATED CO2: A SYNTHESIS OF FOREST FACE EXPERIMENTS

The extent to which greater net primary productivity (NPP) will be sustained as the atmospheric CO2 concentration increases will depend, in part, on the long-term supply of N for plant growth. Over a two-year period, we used common field and laboratory methods to quantify microbial N, gross N mineralization, microbial N immobilization, and specific microbial N immobilization in three free-air CO2 enrichment experiments (Duke Forest, Oak Ridge, Rhinelander). In these experiments, elevated atmospheric CO2 has in- creased the input of above- and belowground litter production, which fuels heterotrophic metabolism in soil. Nonetheless, we found no effect of atmospheric CO2 concentration on any microbial N cycling pool or process, indicating that greater litter production had not initially altered the microbial supply of N for plant growth. Thus, we have no evidence that changes in plant litter production under elevated CO2 will initially slow soil N avail- ability and produce a negative feedback on NPP. Understanding the time scale over which greater plant production modifies microbial N demand lies at the heart of our ability to predict long-term changes in soil N availability and hence whether greater NPP will be sustained in a CO2-enriched atmosphere.

Nitrogen resorption in senescing tree leaves in a warmer, CO2-enriched atmosephere

The prediction that litter quality, and hence litter decomposition rates, would be reduced when plants are grown in a CO2-enriched atmosphere has been based on the observation that foliar N concentrations usually are lower in elevated [CO2]. The implicit assumption is that the N concentration in leaf litter reflects the N concentration in green leaves. Here we evaluate that assumption by exploring whether the process of seasonal nutrient resorption is different in CO2-enriched plants. Nitrogen resorption was studied in two species of maple trees (Acer rubrum L. and A. saccharum Marsh.), which were planted in unfertilized soil and grown in open-top chambers with ambient or elevated [CO2] in combination with ambient or elevated temperature. In the second growing season, prior to autumn senescence, individual leaves were collected and analyzed for N and dry matter content. Other leaves at the same and an adjacent node were collected for analysis as they senesced and abscised. This data set was augmented with litter samples from the first growing season and with green leaves and leaf litter collected from white oak (Quercus alba L.) saplings grown in ambient and elevated [CO2] in open-top chambers. In chambers maintained at ambient temperature, CO2 enrichment reduced green leaf N concentrations by 25% in A. rubrum and 19% in A. saccharum. CO2 enrichment did not significantly reduce resorption efficiency so the N concentration also was reduced in litter. There were, however, few effects of [CO2] on N dynamics in these leaves; differences in N concentration usually were the result of increased dry matter content of leaves. The effects of elevated [CO2] on litter N are inherently more difficult to detect than differences in green leaves because factors that affect senescence and resorption increase variability. This is especially so when other environmental factors cause a disruption in the normal progress of resorption, such as in the first year when warming delayed senescence until leaves were killed by an early frost. The results of this experiment support the approach used in ecosystem models in which resorption efficiency is constant in ambient and elevated [CO2], but the results also indicate that other factors can alter resorption efficiency.