Elevated CO2 and moisture effects on soil carbon storage and cycling in temperate grasslands

In grassland ecosystems, most of the carbon (C) occurs below-ground. Understanding changes in soil fluxes induced by elevated atmospheric CO₂ is critical for balancing the global C budget and for managing grassland ecosystems sustainably. In this review, we use the results of short-term (1–2 years) studies of below-ground processes in grassland communities under elevated CO₂ to assess future prospects for longer-term increases in soil C storage.
Results are broadly consistent with those from other plant communities and include: increases in below-ground net primary productivity and an increase in soil C cycling rate, changes in soil faunal community, and generally no increase in soil C storage. Based on other experimental data, future C storage could be favoured in soils of moderate nutrient status, moderate-to-high clay content, and low (or moderateIy high) soil moisture status. Some support for these suggestions is provided by preliminary results from direct measurements of soil C concentrations near a New Zealand natural CO₂-venting spring, and by simulations of future changes in grassland soils under the combined effects of CO₂ fertilization and regional climate change.
Early detection of any increase in soil C storage appears unlikely in complex grassland communities because of (a) the difficulty of separating an elevated CO₂ effect from the effects of soil factors including moisture status, (b) the high spatial variability of soil C and (c) the effects of global warming. Several research imperatives are identified for reducing the uncertainties in the effects of elevated atmospheric CO₂ on soil C.     

Experimental confirmation of ecosystem model predictions comparing transient and equilibrium plant responses to elevated atmospheric CO2

Ecosystem models predict that short-term responses to elevated atmospheric CO₂ may differ substantially from the "real" long-term responses expected at equilibrium. Experimental validation of these model predictions is difficult as the data available are from short-term studies that do not include biogeochemical feedbacks typical of long-term exposure. Using a reciprocal transplant design at a natural CO₂ spring, we generated combinations of atmospheric and soil conditions that represented both short- and long-term elevated CO₂ conditions. Plant responses were significantly different between these treatments, confirming model predictions that there is not a simple relationship between transient and equilibrium responses to elevated CO₂.     

Respiratory responses of higher plants to atmospheric CO2 enrichment

Although the respiratory response of native and agricultural plants to atmospheric CO₂ enrichment has been reported over the past 75 years, only recently have these effects emerged as prominent measures of plant and ecosystem response to the earth's changing climate. In this review we discuss this rapidly expanding field of study and propose that both increasing and decreasing rates of leaf and whole-plant respiration are likely to occur in response to rising CO₂ concentrations. While the stimulatory effects of CO₂ on respiration are consistent with our knowledge of leaf carbohydrate status and plant metabolism, we wish to emphasize the rather surprising short-term inhibition of leaf respiration by elevated CO₂ and the reported effects of long-term CO₂ exposure on growth and maintenance respiration. As is being found in many studies, it is easier to document the respiratory response of higher plants to elevated CO₂ than it is to assign a mechanistic basis for the observed effects. Despite this gap in our understanding of how respiration is affected by CO₂ enrichment, data are sufficient to suggest that changes in leaf and whole-plant respiration may be important considerations in the carbon dynamics of terrestrial ecosystems as global CO₂ continues to rise. Suggestions for future research that would enable these and other effects of CO₂ on respiration to be unravelled are presented.     

Increased photosynthetic capacity of Scirpus olneyi after 4 years of exposure to elevated CO2

Abstract. While a short-term exposure to elevated atmospheric CO₂ induces a large increase in photosynthesis in many plants, long-term growth in elevated CO₂ often results in a smaller increase due to reduced photosynthetic capacity. In this study, it was shown that, for a wild C₃ species growing in its natural environment and exposed to elevated CO₂ for four growing seasons, the photosynthetic capacity has actually increased by 31%. An increase in photosynthetic capacity has been observed in other species growing in the field, which suggests that photosynthesis of certain field grown plants will continue to respond to elevated levels of atmospheric CO₂     

Soil microbial responses to increased concentrations of atmospheric CO2

Terrestrial ecosystems respond to an increased concentration of atmospheric CO₂. While elevated atmospheric CO₂ has been shown to alter plant growth and productivity, it also affects ecosystem structure and function by changing below-ground processes. Knowledge of how soil microbiota respond to elevated atmospheric CO₂ is of paramount importance for understanding global carbon and nutrient cycling and for predicting changes at the ecosystem-level. An increase in the atmospheric CO₂ concentration not only alters the weight, length, and architecture of plant roots, but also affects the biotic and abiotic environment of the root system. Since the concentration of CO₂ in soil is already 10–50 times higher than that in the atmosphere, it is unlikely that increasing atmospheric CO₂ will directly influence the rhizosphere. Rather, it is more likely that elevated atmospheric CO₂ will affect the microbe–soil–plant root system indirectly by increasing root growth and rhizodeposition rates, and decreasing soil water deficit. Consequently, the increased amounts and altered composition of rhizosphere-released materials will have the potential to alter both population and community structure, and activity of soil- and rhizosphere-associated microorganisms. This occurrence could in turn affect plant health and productivity and plant community structure. This review covers current knowledge about the response of soil microbes to elevated concentrations of atmospheric CO₂.     

Soil CO2 efflux in a boreal pine forest under atmospheric CO2 enrichment and air warming

The response of forest soil CO₂ efflux to the elevation of two climatic factors, the atmospheric concentration of CO₂ (↑CO₂ of 700 μmol mol⁻¹) and air temperature (↑ T with average annual increase of 5°C), and their combination (↑CO₂+↑ T ) was investigated in a 4-year, full-factorial field experiment consisting of closed chambers built around 20-year-old Scots pines ( Pinus sylvestris L.) in the boreal zone of Finland. Mean soil CO₂ efflux in May–October increased with elevated CO₂ by 23–37%, with elevated temperature by 27–43%, and with the combined treatment by 35–59%. Temperature elevation was a significant factor in the combined 4-year efflux data, whereas the effect of elevated CO₂ was not as evident. Elevated temperature had the most pronounced impact early and late in the season, while the influence of elevated CO₂ alone was especially notable late in the season. Needle area was found to be a significant predictor of soil CO₂ efflux, particularly in August, a month of high root growth, thus supporting the assumption of a close link between whole-tree physiology and soil CO₂ emissions. The decrease in the temperature sensitivity of soil CO₂ efflux observed in the elevated temperature treatments in the second year nevertheless suggests the existence of soil response mechanisms that may be independent of the assimilating component of the forest ecosystem. In conclusion, elevated atmospheric CO₂ and air temperature consistently increased forest soil CO₂ efflux over the 4-year period, their combined effect being additive, with no apparent interaction.     

Influences of soil volume and an elevated CO2 level on growth and CO2 exchange for the Crassulacean acid metabolism plant Opuntia ficus-indica

Effects of the current (38 Pa) and an elevated (74 Pa) CO₂ partial pressure on root and shoot areas, biomass accumulation and daily net CO₂ exchange were determined for Opuntia ficus-indica (L.) Miller, a highly productive Crassulacean acid metabolism species cultivated worldwide. Plants were grown in environmentally controlled rooms for 18 weeks in pots of three soil volumes (2 600, 6 500 and 26 000 cm³), the smallest of which was intended to restrict root growth. For plants in the medium-sized soil volume, basal cladodes tended to be thicker and areas of main and lateral roots tended to be greater as the CO₂ level was doubled. Daughter cladodes tended to be initiated sooner at the current compared with the elevated CO₂ level but total areas were similar by 10 weeks. At 10 weeks, daily net CO₂ uptake for the three soil volumes averaged 24% higher for plants growing under elevated compared with current CO₂ levels, but at 18 weeks only 3% enhancement in uptake occurred. Dry weight gain was enhanced 24% by elevated CO₂ during the first 10 weeks but only 8% over 18 weeks. Increasing the soil volume 10-fold led to a greater stimulation of daily net CO₂ uptake and biomass production than did doubling the CO₂ level. At 18 weeks, root biomass doubled and shoot biomass nearly doubled as the soil volume was increased 10-fold; the effects of soil volume tended to be greater for elevated CO₂. The amount of cladode nitrogen per unit dry weight decreased as the CO₂ level was raised and increased as soil volume increased, the latter suggesting that the effects of soil volume could be due to nitrogen limitations.     

Sensing of atmospheric CO2 by plants

Abstract. Despite recent interest in the effects of high CO₂ on plant growth and physiology, very little is known about the mechanisms by which plants sense changes in the concentration of this gas. Because atmospheric CO₂ concentration is relatively constant and because the conductance of the cuticle to CO₂ is low, sensory mechanisms are likely to exist only for intercellular CO₂ concentration. Therefore, responses of plants to changes in atmospheric CO₂ will depend on the effect of these changes on intercellular CO₂ concentration. Although a variety of plant responses to atmospheric CO₂ concentration have been reported, most of these can be attributed to the effects of intercellular CO₂ on photosynthesis or stomatal conductance. Short-term and long-term effects of CO₂ on photosynthesis and stomatal conductance are discussed as sensory mechanisms for responses of plants to atmospheric CO₂. Available data suggest that plants do not fully realize the potential increases in productivity associated with increased atmospheric CO₂. This may be because of genetic and environmental limitations to productivity or because plant responses to CO₂ have evolved to cope with variations in intercellular CO₂ caused by factors other than changes in atmospheric CO₂.     

Evolutionary responses of stomatal density to global CO2 change

Stomatal density is known to respond to CO₂ levels during leaf development. Current interest in the increasing concentration of atmospheric CO₂ has stimulated much experimentation on the responses of plants to relatively short-term exposure in artificially high CO₂ levels. Attempts to extrapolate from short-term to long-term responses raise fundamental questions concerning evolutionary change in response to rising global CO₂ levels. We consider the improved water use efficiency observed under elevated CO₂ levels to be the main driving force of natural selection affecting the genotypic component controlling stomatal density. Whether a response is merely phenotypic or becomes incorporated into the genotype depends on two factors: (i) the time scale of exposure and (ii) the generation time of a species. Measurements of stomatal density on fossil leaves of Salix herbacea through a glacial cycle covering the last 140000 years have shown a decrease in stomatal density in response to the rising CO₂ levels of this period. This accords with the shorter-term observations on leaves of trees seen in herbarium specimens where the stomatal density has decreased in response to the rising CO₂ levels of the last 200 years. The results indicate that natural selection over the 140000-year period may have favoured a similar response to that shown by trees phenotypically over the last 200 years. Since there is now some evidence for the genetic control of stomatal density, the role of natural selection affecting it must be considered when translating responses from short-term experiments to predict how stomatal density will be affected by long-term climatic and atmospheric change.     

Elevated CO2 concentrations and stomatal density: observations from 17 plant species growing in a CO2 spring in central Italy

Stomatal density (SD) and stomatal conductance ( g _s) can be affected by an increase of atmospheric CO₂ concentration. This study was conducted on 17 species growing in a naturally enriched CO₂ spring and belonging to three plant communities. Stomatal conductance, stomatal density and stomatal index (SI) of plants from the spring, which were assumed to have been exposed for generations to elevated [CO₂], and of plants of the same species collected in a nearby control site, were compared. Stomatal conductance was significantly lower in most of the species collected in the CO₂ spring and this indicated that CO₂ effects on g _s are not of a transitory nature but persist in the long term and through plant generations. Such a decrease was, however, not associated with changes in the anatomy of leaves: SD was unaffected in the majority of species (the decrease was only significant in three out of the 17 species examined), and also SI values did not vary between the two sites with the exception of two species that showed increased SI in plants grown in the CO₂-enriched area. These results did not support the hypothesis that long-term exposure to elevated [CO₂] may cause adaptive modification in stomatal number and in their distribution.     

Effects of long-term elevated [CO2] from natural CO2 springs on Nardus stricta: photosynthesis, biochemistry, growth and phenology

Plants of Nardus stricta growing near a cold, naturally emitting CO₂ spring in Iceland were used to investigate the long-term (> 100 years) effects of elevated [CO₂] on photosynthesis, biochemistry, growth and phenology in a northern grassland ecosystem. Comparisons were made between plants growing in an atmosphere naturally enriched with CO₂ (≈ 790 μ mol mol^–1) near the CO₂ spring and plants of the same species growing in adjacent areas exposed to ambient CO₂ concentrations (≈360 μ mol mol^–1). Nardus stricta growing near the spring exhibited earlier senescence and reductions in photosynthetic capacity (≈25%), Rubisco content (≈26%), Rubisco activity (≈40%), Rubisco activation state (≈23%), chlorophyll content (≈33%) and leaf area index (≈22%) compared with plants growing away from the spring. The potential positive effects of elevated [CO₂] on grassland ecosystems in Iceland are likely to be reduced by strong down-regulation in the photosynthetic apparatus of the abundant N. stricta species.     

Effects of source-sink relations on photosynthetic acclimation to elevated CO2

Abstract. While photosynthesis of C₃ plants is stimulated by an increase in the atmospheric CO₂ concentration, photosynthetic capacity is often reduced after long-term exposure to elevated CO₂. This reduction appears to be brought about by end product inhibition, resulting from an imbalance in the supply and demand of carbohydrates. A review of the literature revealed that the reduction of photosynthetic capacity in elevated CO₂ was most pronounced when the increased supply of carbohydrates was combined with small sink size. The volume of pots in which plants were grown affected the sink size by restricting root growth. While plants grown in small pots had a reduced photosynthetic capacity, plants grown in the field showed no reduction or an increase in this capacity. Pot volume also determined the effect of elevated CO₂ on the root/shoot ratio: the root/shoot ratio increased when root growth was not restricted and decreased in plants grown in small pots. The data presented in this paper suggest that plants growing in the field will maintain a high photosynthetic capacity as the atmospheric CO₂ level continues to rise.     

Carbon gains by desiccation-tolerant plants at elevated CO2

1. There have been no reports of the long-term responses of the desiccation-tolerant (DT) plants to elevated CO₂. Xerophyta scabrida is a DT woody shrub, which loses chlorophylls and thylakoids during desiccation: a so-called poikilochlorophyllous desiccation-tolerant species (PDT). When the leaves of X. scabria are allowed to desiccate, the species shows many of the normal features of (P)DT plants.
2. However, the duration of photosynthesis in X. scabria is prolonged by 300% when the measurements are made at 700 as opposed to 350p.p.m. CO₂. The implication is that the carboxylating enzymes must still have been active at this time to enable appreciable photosynthetic activity. This response could have far-reaching implications for the success of such species in a future climate.
3. Lichens and mosses, representing the homoiochlorophyllous DTs (HDT), retain their chlorophyll content and photosynthetic apparatus during desiccation. We show the desiccation responses of two common HDT species ( Cladonia convoluta and Tortula ruralis ) to elevated CO₂ for comparison. Both HDT species showed increased net CO₂ uptake in the material grown at high CO₂ by more than 30% in moss and by more than 50% in lichen. It is concluded that desiccation-tolerant plants will be among the main beneficiaries of a high CO₂ future.     

Effect of enhanced atmospheric CO2 on mycorrhizal colonization by Glomus mosseae in Plantago lanceolata and Trifolium repens

Plantago lanceolata L. and Trifolium repens L. were grown for 16 wk in ambient (360 μmol mol⁻¹) and elevated (610 μmol mol⁻¹) atmospheric CO₂. Plants were inoculated with the arbuscular mycorrhizal (AM) fungus Glomus mosseae (Nicol. & Gerd.) Gerdemann & Trappe and given a phosphorus supply in the form of bonemeal, which would not be immediately available to the plants. Seven sequential harvests were taken to determine whether the effect of elevated CO₂ on mycorrhizal colonization was independent of the effect of CO₂ on plant growth. Plant growth analysis showed that both species grew faster in elevated CO₂ and that P. lanceolata had increased carbon allocation towards the roots. Elevated CO₂ did not affect the percentage of root length colonized (RLC); although total colonized root length was greater, when plant size was taken into account this effect disappeared. This finding was also true for root length colonized by arbuscules. No CO₂ effect was found on hyphal density (colonization intensity) in roots. The P content of plants was increased at elevated CO₂, although both shoot and root tissue P concentration were unchanged. This was again as a result of bigger plants at elevated CO₂. Phosphorus inflow was unaffected by CO₂ concentrations. It is concluded that there is no direct permanent effect of elevated CO₂ on mycorrhizal functioning, as internal mycorrhizal development and the mycorrhizal P uptake mechanism are unaffected. The importance of sequential harvests in experiments is discussed. The direction for future research is highlighted, especially in relation to C storage in the soil.     

The response of nodulated alfalfa to water supply, temperature and elevated CO2: photosynthetic downregulation

Plants grown in an environment of elevated CO₂ and temperature often show reduced CO₂ assimilation capacity, providing evidence of photosynthetic downregulation. The aim of this study was to analyse the downregulation of photosynthesis in elevated CO₂ (700 µmol mol⁻¹) in nodulated alfalfa plants grown at different temperatures (ambient and ambient + 4°C) and water availability regimes in temperature gradient tunnels. When the measurements were taken in growth conditions, a combination of elevated CO₂ and temperature enhanced the photosynthetic rate; however, when they were carried out at the same CO₂ concentration (350 and 700 µmol mol⁻¹), elevated CO₂ induced photosynthetic downregulation, regardless of temperature and drought. Intercellular CO₂ concentration measurements revealed that photosynthetic acclimation could not be accounted for by stomatal limitations. Downregulation of plants grown in elevated CO₂ was a consequence of decreased carboxylation efficiency as a result of reduced rubisco activity and protein content; in plants grown at ambient temperature, downregulation was also induced by decreased quantum efficiency. The decrease in rubisco activity was associated with carbohydrate accumulation and depleted nitrogen availability. The root nodules were not sufficiently effective to balance the source–sink relation in elevated CO₂ treatments and to provide the required nitrogen to counteract photosynthetic acclimation.     

Effect of elevated CO2, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle

Rising atmospheric CO₂ may increase potential net leaf photosynthesis under short-term exposure, but this response decreases under long-term exposure because plants acclimate to elevated CO₂ concentrations through a process known as downregulation. One of the main factors that may influence this phenomenon is the balance between sources and sinks in the plant. The usual method of managing a forage legume like alfalfa requires the cutting of shoots and subsequent regrowth, which alters the source/sink ratio and thus photosynthetic behaviour. The aim of this study was to determine the effect of CO₂ (ambient, around 350 vs. 700 µmol mol⁻¹), temperature (ambient vs. ambient + 4° C) and water availability (well-irrigated vs. partially irrigated) on photosynthetic behaviour in nodulated alfalfa before defoliation and after 1 month of regrowth. At the end of vegetative normal growth, plants grown under conditions of elevated CO₂ showed photosynthetic acclimation with lower photosynthetic rates, V_cmax and ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) activity. This decay was probably a consequence of a specific rubisco protein reduction and/or inactivation. In contrast, high CO₂ during regrowth did not change net photosynthetic rates or yield differences in V_cmax or rubisco total activity. This absence of photosynthetic acclimation was directly associated with the new source-sink status of the plants during regrowth. After cutting, the higher root/shoot ratio in plants and remaining respiration can function as a strong sink for photosynthates, avoiding leaf sugar accumulation, the negative feed-back control of photosynthesis, and as a consequence, photosynthetic downregulation.     

Foliar antioxidant status of plants from naturally high‐CO2 sites

We compared the foliar antioxidant status of native Agrostis stolonifera L. communities growing at two distinct CO₂‐enriched sites of geothermal origin (E) and at a control field location with normal CO₂. Compared to the control, plants from both E‐sites showed an increased size of the GSH pool, essentially due to enhanced GSSG levels, and a consequent decrease in the ratio between reduced and oxidised glutathione forms. Such differences were maintained and even enhanced in the vegetatively‐propagated progenies of control and E‐plants, grown under both greenhouse conditions and normal CO₂ levels. The above results confirmed previous observations on native and crop plants exposed to elevated CO₂. It is therefore suggested that changes in the glutathione redox balance might be of adaptive significance under conditions of permanent exposure to high CO₂.     

In situ responses to elevated CO2 in tropical forest understorey plants

1. Plants growing in deep shade and high temperature, such as in the understorey of humid tropical forests, have been predicted to be particularly sensitive to rising atmospheric CO₂. We tested this hypothesis in five species whose microhabitat quantum flux density (QFD) was documented as a covariable. After 7 (tree seedlings of Tachigalia versicolor and Beilschmiedia pendula ) and 18 months (shrubs Piper cordulatum and Psychotria limonensis, and grass Pharus latifolius ) of elevated CO₂ treatment ( c. 700 μl litre^–1) under mean QFD of less than 11 μmol m^–2 s^–1, all species produced more biomass (25–76%) under elevated CO₂.
2. Total plant biomass tended to increase with microhabitat QFD (daytime means varying from 5 to 11μmol m^–2 s^–1) but the relative stimulation by elevated CO₂ was higher at low QFD except in Pharus .
3. Non-structural carbohydrate concentrations in leaves increased significantly in Pharus (+ 27%) and Tachigalia (+ 40%).
4. The data support the hypothesis that tropical plants growing near the photosynthetic light compensation point are responsive to elevated CO₂. An improved plant carbon balance in deep shade is likely to influence understorey plant recruitment and competition as atmospheric CO₂ continues to rise.     

Stimulation of r- vs. K-selected microorganisms by elevated atmospheric CO2 depends on soil aggregate size

Increased root exudation under elevated atmospheric CO₂ and the contrasting environments in soil macro- and microaggregates could affect microbial growth strategies. We investigated the effect of elevated CO₂ on the contribution of fast- ( r -strategists) and slow-growing ( K -strategists) microorganisms in soil macro- and microaggregates. We fractionated the bulk soil from the ambient and elevated (for 5 years) CO₂ treatments of FACE-Hohenheim (Stuttgart) into large macro- (>2 mm), small macro- (0.25–2.00 mm), and microaggregates (<0.25 mm) using 'optimal moist' sieving. Microbial biomass (C_mic), the maximum specific growth rate (μ), growing microbial biomass (GMB) and lag-period ( t _lag) were estimated by the kinetics of CO₂ emission from bulk soil and aggregates amended with glucose and nutrients. Although C_org and C_mic were unaffected by elevated CO₂, μ values were significantly higher under elevated than ambient CO₂ for bulk soil, small macroaggregates, and microaggregates. Substrate-induced respiratory response increased with decreasing aggregate size under both CO₂ treatments. Based on changes in μ, GMB and lag period, we conclude that elevated atmospheric CO₂ stimulated the r- selected microorganisms, especially in soil microaggregates. Such an increase in r -selected microorganisms indicates acceleration of available C mineralization in soil, which may counterbalance the additional C input by roots in soils in a future elevated atmospheric CO₂ environment.     

Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition

In this review, we discuss the potential for mycorrhizal fungi to act as a source or sink for carbon (C) under elevated CO₂ and nitrogen deposition. Mycorrhizal tissue has been estimated to comprise a significant fraction of soil organic matter and below-ground biomass in a range of systems. The current body of literature indicates that in many systems exposed to elevated CO₂, mycorrhizal fungi might sequester increased amounts of C in living, dead and residual hyphal biomass in the soil. Through this process, the fungi might serve as a negative feedback on the rise in atmospheric CO₂ levels caused by fossil fuel burning and deforestation. By contrast, a few preliminary studies suggest that N deposition might increase turnover rates of fungal tissue and negate CO₂ effects on hyphal biomass. If these latter responses are consistent among ecosystems, C storage in hyphae might decline in habitats surrounding agricultural and urban areas. When N additions occur without CO₂ enrichment, effects on mycorrhizal growth are inconsistent. We note that analyses of hyphal decomposition under elevated CO₂ and N additions are extremely sparse but are critical in our understanding of the impact of global change on the cycling of mycorrhizal C. Finally, shifts in the community composition of arbuscular and ectomycorrhizal fungi with increasing CO₂ or N availability are frequently documented. Since mycorrhizal groups vary in growth rate and tissue quality, these changes in species assemblages could produce unforeseeable impacts on the productivity, survivorship, or decomposition of mycorrhizal biomass.