Modeling the belowground response of plants and soil biota to edaphic and climatic change—What can we expect to gain?

As atmospheric CO₂ concentrations continue to increase, so too will the emphasis placed on understanding the belowground response of plants to edaphic and climatic change. Controlled-exposure studies that address the significance of an increased supply of carbon to roots and soil biota, and the consequences of this to nutrient cycling will play a prominent role in this process. Models will also contribute to understanding the response of plants and ecosystems to changes in the earth's climate by incorporating experimental results into conceptual or quantitative frameworks from which potential feedbacks within the plant-soil system can be identified. Here we present five examples of how models can be used in this analysis and how they can contribute to the development of new hypotheses in the areas of root biology, soil biota, and ecosystem processes. Two examples illustrate the role of coarse and fine roots in nitrogen and phosphorus uptake from soils, the respiratory costs associated with this acquisition of nutrients, and the significance of root architecture in these relationships. Another example focuses on a conceptual model that has helped raise new ideas about the effects of elevated CO₂ on root and microbial biomass, and on nutrient dynamics in the rhizosphere. Difficulties associated with modeling the contribution of mycorrhizal fungi to whole-plant growth are also discussed. Finally, several broad-scale models are used to illustrate the importance of root turnover, litter decomposition, and nitrogen mineralization in determining an ecosystem's response to atmospheric CO₂ enrichment. We conclude that models are appropriate tools for use both in guiding existing studies and in identifying new hypotheses for future research. Development of models that address the complexities of belowground processes and their role in determining plant and ecosystem function within the context of rising CO₂ concentrations and associated climate change should be encouraged.     

Effects of enhanced atmospheric CO2 and nutrient supply on the quality and subsequent decomposition of fine roots of Betula pendula Roth. and Picea sitchensis (Bong.) Carr.

Fine root litter derived from birch (Betula pendula Roth.) and Sitka spruce (Picea sitchensis (Bong.) Carr.) plants grown under two CO₂ atmospheric concentrations (350 ppm and 600 ppm) and two nutrient regimes was used for decomposition studies in laboratory microcosms. Although there were interactions between litter type, CO₂/fertiliser treatments and decomposition rates, in general, an increase in the C/N ratio of the root tissue was observed for roots of both species grown under elevated CO₂ in unfertilized soil. Both weight loss and respiration of decomposing birch roots were significantly reduced in materials derived from enriched CO₂, whilst the decomposition of spruce roots showed no such effect. A parallel experiment was performed using Betula pendula root litter grown under different N regimes, in order to test the relationship between C/N ratio of litter and root decomposition rate. A highly significant (p<0.001) negative correlation between C/N ratio and root litter respiration was found, with an r²=0.97. The results suggest that the increased C/N ratio of plant tissues induced by elevated CO₂ can result in a reduction of decomposition rate, with a resulting increase in forest soil C stores.     

Nitrogen deposition and plant species interact to influence soil carbon stabilization

Anthropogenic nitrogen (N) deposition effects on soil organic carbon (C) decomposition remain controversial, while the role of plant species composition in mediating effects of N deposition on soil organic C decomposition and long‐term soil C sequestration is virtually unknown. Here we provide evidence from a 5‐year grassland field experiment in Minnesota that under elevated atmospheric CO₂ concentration (560 ppm), plant species determine whether N deposition inhibits the decomposition of soil organic matter via inter‐specific variation in root lignin concentration. Plant species producing lignin‐rich litter increased stabilization of soil C older than 5 years, but only in combination with elevated N inputs (4 g m^?2 year^?1). Our results suggest that N deposition will increase soil C sequestration in those ecosystems where vegetation composition and/or elevated atmospheric CO₂ cause high litter lignin inputs to soils.     

Elevated CO2 reduces field decomposition rates of Betula pendula (Roth.) leaf litter

The effect of elevated atmospheric CO₂ and nutrient supply on elemental composition and decomposition rates of tree leaf litter was studied using litters derived from birch (Betula pendula Roth.) plants grown under two levels of atmospheric CO₂ (ambient and ambient +250 ppm) and two nutrient regimes in solar domes. CO₂ and nutrient treatments affected the chemical composition of leaves, both independently and interactively. The elevated CO₂ and unfertilized soil regime significantly enhanced lignin/N and C/N ratios of birch leaves. Decomposition was studied using field litter-bags, and marked differences were observed in the decomposition rates of litters derived from the two treatments, with the highest weight remaining being associated with litter derived from the enhanced CO₂ and unfertilized regime. Highly significant correlations were shown between birch litter decomposition rates and lignin/N and C/N ratios. It can be concluded, from this study, that at levels of atmospheric CO₂ predicted for the middle of the next century a deterioration of litter quality will result in decreased decomposition rates, leading to reduction of nutrient mineralization and increased C storage in forest ecosystems. However, such conclusions are difficult to generalize, since tree responses to elevated CO₂ depend on soil nutritional status.     

13C and 15N in microarthropods reveal little response of Douglas-fir ecosystems to climate change

Understanding ecosystem carbon (C) and nitrogen (N) cycling under global change requires experiments maintaining natural interactions among soil structure, soil communities, nutrient availability, and plant growth. In model Douglas-fir ecosystems maintained for five growing seasons, elevated temperature and carbon dioxide (CO₂) increased photosynthesis and increased C storage belowground but not aboveground. We hypothesized that interactions between N cycling and C fluxes through two main groups of microbes, mycorrhizal fungi (symbiotic with plants) and saprotrophic fungi (free-living), mediated ecosystem C storage. To quantify proportions of mycorrhizal and saprotrophic fungi, we measured stable isotopes in fungivorous microarthropods that efficiently censused the fungal community. Fungivorous microarthropods consumed on average 35% mycorrhizal fungi and 65% saprotrophic fungi. Elevated temperature decreased C flux through mycorrhizal fungi by 7%, whereas elevated CO₂ increased it by 4%. The dietary proportion of mycorrhizal fungi correlated across treatments with total plant biomass (n= 4, r²= 0.96, P= 0.021), but not with root biomass. This suggests that belowground allocation increased with increasing plant biomass, but that mycorrhizal fungi were stronger sinks for recent photosynthate than roots. Low N content of needles (0.8–1.1%) and A horizon soil (0.11%) coupled with high C : N ratios of A horizon soil (25–26) and litter (36–48) indicated severe N limitation. Elevated temperature treatments increased the saprotrophic decomposition of litter and lowered litter C : N ratios. Because of low N availability of this litter, its decomposition presumably increased N immobilization belowground, thereby restricting soil N availability for both mycorrhizal fungi and plant growth. Although increased photosynthesis with elevated CO₂ increased allocation of C to ectomycorrhizal fungi, it did not benefit plant N status. Most N for plants and soil storage was derived from litter decomposition. N sequestration by mycorrhizal fungi and limited N release during litter decomposition by saprotrophic fungi restricted N supply to plants, thereby constraining plant growth response to the different treatments.     

Leaf litter production and decomposition in a poplar short-rotation coppice exposed to free air CO2 enrichment (POPFACE)

The capacity of forest ecosystems to sequester C in the soil relies on the net balance between litter production above, as well as, below ground, and decomposition processes. Nitrogen mineralization and its availability for plant growth and microbial activity often control the speed of both processes. Litter production, decomposition and N mineralization are strongly interdependent. Thus, their responses to global environmental changes (i.e. elevated CO₂, climate, N deposition, etc.) cannot be fully understood if they are studied in isolation. In the present experiment, we investigated litter fall, litter decomposition and N dynamics in decomposing litter of three Populus spp., in the second and third growing season of a short rotation coppice under FACE. Elevated CO₂ did not affect annual litter production but slightly retarded litter fall in the third growing season. In all species, elevated CO₂ lowered N concentration, resulting in a reduction of N input to the soil via litter fall, but did not affect lignin concentrations. Litter decomposition was studied in bags incubated in situ both in control and FACE plots. Litter lost between 15% and 18% of the original mass during the eight months of field incubation. On average, litter produced under elevated CO₂ attained higher residual mass than control litter. On the other end, when litter was incubated in FACE plots it exhibited higher decay rates. These responses were strongly species‐specific. All litter increased their N content during decomposition, indicating immobilization of N from external sources. Independent of the initial quality, litter incubated on FACE soils immobilized less N, possibly as a result of lower N availability in the soil. Indeed, our results refer to a short‐term decomposition experiment. However, according to a longer‐term model extrapolation of our results, we anticipate that in Mediterranean climate, under elevated atmospheric CO₂, soil organic C pool of forest ecosystems may initially display faster turnover, but soil N availability will eventually limit the process.     

Decomposability of C3 and C4 grass litter sampled under different concentrations of atmospheric carbon dioxide at a natural CO2 spring

Elevated concentrations of atmospheric CO₂ can influence the relative proportions, biomass and chemical composition of plant species in an ecosystem and, thereby, the input of litter nutrients to soil. Plant growth under elevated CO₂ appears to have no consistent effect on rates of litter decomposition; decomposition can, however, differ in C3 and C4 plant material from the same CO₂ environment. We here describe the decomposability of leaf litter of two grass species – the C3 Holcus lanatus L. (Yorkshire fog) and C4 Pennisetum clandestinum Hochst. (kikuyu) - from an unfertilized, ungrazed grassland at a cold CO₂ spring in Northland, New Zealand. Decomposability was measured by net CO₂–C production from litter incubated for 56 days at 25 °C in a gley soil from the site; net mineral-N production from litter was also determined. Both litter and soils were sampled under `low' and `high' concentrations of atmospheric CO₂. Decomposition of H. lanatus litter was greater than that of P. clandestinum litter throughout the 56-day incubation. Decomposition tended to be greater in `high-CO<sub>2</sub>' than in `low-CO₂' H. lanatus litter, but lower in `high-CO<sub>2</sub>' than `low-CO₂' P. clandestinum litter; differences were, however, non-significant after 28 days. Overall, litter decomposition was greater in the `low-CO<sub>2</sub>' than `high-CO₂' soil. Differences in decomposition rates were related negatively to litter N concentrations and positively to C:N ratios, but were not predictable from lignin:total N ratios. Net mineral-N production from litter decomposition did not differ significantly in `high-CO<sub>2</sub>' and `low-CO₂' samples incubated in `low-CO<sub>2</sub>' soil; in `high-CO₂' soil some net immobilization was observed. Overall, results indicate the likely complexity of litter decomposition in the field but, nevertheless, strongly suggest that rates of decomposition will not necessarily decline in a `high-CO₂' environment.     

Elevated CO2 and temperature impacts on different components of soil CO2 efflux in Douglas-fir terracosms

Although numerous studies indicate that increasing atmospheric CO₂ or temperature stimulate soil CO₂ efflux, few data are available on the responses of three major components of soil respiration [i.e. rhizosphere respiration (root and root exudates), litter decomposition, and oxidation of soil organic matter] to different CO₂ and temperature conditions. In this study, we applied a dual stable isotope approach to investigate the impact of elevated CO₂ and elevated temperature on these components of soil CO₂ efflux in Douglas-fir terracosms. We measured both soil CO₂ efflux rates and the ¹³C and ¹⁸O isotopic compositions of soil CO₂ efflux in 12 sun-lit and environmentally controlled terracosms with 4-year-old Douglas fir seedlings and reconstructed forest soils under two CO₂ concentrations (ambient and 200 ppmv above ambient) and two air temperature regimes (ambient and 4 °C above ambient). The stable isotope data were used to estimate the relative contributions of different components to the overall soil CO₂ efflux. In most cases, litter decomposition was the dominant component of soil CO₂ efflux in this system, followed by rhizosphere respiration and soil organic matter oxidation. Both elevated atmospheric CO₂ concentration and elevated temperature stimulated rhizosphere respiration and litter decomposition. The oxidation of soil organic matter was stimulated only by increasing temperature. Release of newly fixed carbon as root respiration was the most responsive to elevated CO₂, while soil organic matter decomposition was most responsive to increasing temperature. Although some assumptions associated with this new method need to be further validated, application of this dual-isotope approach can provide new insights into the responses of soil carbon dynamics in forest ecosystems to future climate changes.     

Effects of elevated [CO2] on forest growth and carbon storage: a modelling analysis of the consequences of changes in litter quality/quantity and root exudation

Many researchers have proposed that the stimulus of plant growth under elevated [CO₂] observed in short-term experiments will be moderated in the longer term by a reduction in soil nitrogen (N) availability linked to decreased litter quality and/or increased litter production. However, these negative feedbacks may be offset to some extent by a stimulus in N fixation linked to increased root exudation. The aim of this modelling study is to examine how changes in litter quality/quantity and root exudation –- if they occur –- will affect the CO₂ responses of net primary productivity and ecosystem carbon (C) storage on different timescales. We apply a model of C and N cycling in forest ecosystems (G’DAY) to stands of Norway spruce (Picea abies, L. Cast) growing at a N-limited experimental site at Flakaliden, Sweden, and draw the following conclusions: (1) in the absence of changes in litter quality and root exudation, the short-term CO₂ stimulus of litter quantity leads to only a minimal CO₂ stimulus of productivity or C storage in the medium term (≈ 20 years) and long term (≈ 200 years), because of constraints on soil N availability; (2) increasing plant nitrogen use efficiency (via a decrease in the N:C ratio of new litter) makes little impact on these results; (3) a significant CO₂ response in the medium term requires a substantial decrease in the N:C ratio of older litter, when it is approaching stabilisation as soil organic matter, although the long-term CO₂ response remains small; and (4) an increase in N fixation leads to a small effect on productivity in the short term, but a very large effect on both productivity and C storage in the long term. These results suggest that soil N constraints on the long-term CO₂-fertilisation effect can be overcome to a significant extent only by increases in N acquisition, although only modest increases may be required. This revised version was published online in June 2006 with corrections to the Cover Date.     

Chemistry and decomposition of litter from Populus tremuloides Michaux grown at elevated atmospheric CO2 and varying N availability

It has been hypothesized that greater production of total nonstructural carbohydrates (TNC) in foliage grown under elevated atmospheric carbon dioxide (CO₂) will result in higher concentrations of defensive compounds in tree leaf litter, possibly leading to reduced rates of decomposition and nutrient cycling in forest ecosystems of the future. To evaluate the effects of elevated atmospheric CO₂ on litter chemistry and decomposition, we performed a 111 day laboratory incubation with leaf litter of trembling aspen (Populus tremuloides Michaux) produced at 36 Pa and 56 Pa CO₂ and two levels of soil nitrogen (N) availability. Decomposition was quantified as microbially respired CO₂ and dissolved organic carbon (DOC) in soil solution, and concentrations of nonstructural carbohydrates, N, carbon (C), and condensed tannins were monitored throughout the incubation. Growth under elevated atmospheric CO₂ did not significantly affect initial litter concentrations of TNC, N, or condensed tannins. Rates of decomposition, measured as both microbially respired CO₂ and DOC did not differ between litter produced under ambient and elevated CO₂. Total C lost from the samples was 38 mg g^?1 litter as respired CO₂ and 138 mg g^?1 litter as DOC, suggesting short‐term pulses of dissolved C in soil solution are important components of the terrestrial C cycle. We conclude that litter chemistry and decomposition in trembling aspen are minimally affected by growth under higher concentrations of CO₂.