Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal

As C(3) photosynthesis is not yet CO(2)-saturated, forests offer the possibility of enhanced growth and carbon (C) sequestration with rising atmospheric CO(2). However, at an ecosystem scale, increased photosynthetic rates are not always translated into faster tree growth, and in free air carbon enrichment (FACE) experiments with trees, the stimulation in above-ground growth often declines with time. So is tree growth C-limited? The evidence is reviewed here at three different scales. First, at the biochemical scale, the role of Rubisco is discussed by considering its evolution and role as a nitrogen (N) storage protein. Second, at the ecophysiological scale, C allocation to gain nutrients from the soil is considered and it is argued that any C limitation is only through a limitation to soil nutrient cycling. Finally, the response of forest ecosystems to rising atmospheric CO(2) concentrations is considered and evidence from FACE experiments is discussed. From the three lines of evidence we conclude that the growth of trees is not C-limited, with the key to understanding future responses to climate change being turnover of soil organic matter and nutrient cycling.     

Species of plants and associated arbuscular mycorrhizal fungi mediate mycorrhizal responses to CO2 enrichment

It has been suggested that enrichment of atmospheric CO₂ should alter mycorrhizal function by simultaneously increasing nutrient‐uptake benefits and decreasing net C costs for host plants. However, this hypothesis has not been sufficiently tested. We conducted three experiments to examine the impacts of CO₂ enrichment on the function of different combinations of plants and arbuscular mycorrhizal (AM) fungi grown under high and low soil nutrient availability. Across the three experiments, AM function was measured in 14 plant species, including forbs, C₃ and C₄ grasses, and plant species that are typically nonmycorrhizal. Five different AM fungal communities were used for inoculum, including mixtures of Glomus spp. and mixtures of Gigasporaceae (i.e. Gigaspora and Scutellospora spp.). Our results do not support the hypothesis that CO₂ enrichment should consistently increase plant growth benefits from AM fungi, but rather, we found CO₂ enrichment frequently reduced AM benefits. Furthermore, we did not find consistent evidence that enrichment of soil nutrients increases plant growth responses to CO₂ enrichment and decreases plant growth responses to AM fungi. Our results show that the strength of AM mutualisms vary significantly among fungal and plant taxa, and that CO₂ levels further mediate AM function. In general, when CO₂ enrichment interacted with AM fungal taxa to affect host plant dry weight, it increased the beneficial effects of Gigasporaceae and reduced the benefits of Glomus spp. Future studies are necessary to assess the importance of temperature, irradiance, and ambient soil fertility in this response. We conclude that the affects of CO₂ enrichment on AM function varies with plant and fungal taxa, and when making predictions about mycorrhizal function, it is unwise to generalize findings based on a narrow range of plant hosts, AM fungi, and environmental conditions.     

Ectomycorrhizal fungi associated with Pinus sylvestris seedlings respond differently to increased carbon and nitrogen availability: implications for ecosystem responses to global change

The ectomycorrhizal (ECM) symbiosis can cause both positive and negative feedback with trees under elevated CO₂. Positive feedback arises if the additional carbon (C) increases both nutrient uptake by the fungus and nutrient transfer to the plant, whereas negative feedback results from increased nutrient uptake and immobilization by the fungus and reduced transfer to the plant. Because species of ECM fungi differ in their C and nitrogen (N) demand, understanding fungal species‐specific responses to variation in C and N supply is essential to predict impacts of global change. We investigated fungal species‐specific responses of ECM Scots pine (Pinus sylvestris) seedlings under ambient and elevated CO₂ (350 or 700 μL L⁻¹ CO₂) and under low and high mineral N availability. Each seedling was associated with one of the following ECM species: Hebeloma cylindrosporum, Laccaria bicolor and Suillus bovinus. The experiment lasted 103 days. During the final 27 days, seedlings were labeled with ¹⁴CO₂ and ¹⁵N. Most plant and fungal parameters were significantly affected by fungal species, CO₂ level and N supply. Interactions between fungal species and CO₂ were also regularly significant. At low N availability, elevated CO₂ had the smallest impact on the photosynthetic performance of seedlings inoculated with H. cylindrosporum and the largest impact on seedlings with S. bovinus. At ambient CO₂, increasing N supply had the smallest impact on seedlings inoculated with S. bovinus and the largest on seedlings inoculated with H. cylindrosporum. At low N availability, extraradical hyphal length increased after doubling CO₂ level, but this was significant only for L. bicolor. At ambient CO₂, increasing N levels reduced hyphal length for both H. cylindrosporum and S. bovinus, but not for L. bicolor. We discuss the potential interplay of two major elements of global change, elevated CO₂ and increased N availability, and their effects on plant growth. We conclude that increased N supply potentially relieves mycorrhiza‐induced progressive N limitation under elevated CO₂.     

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.     

Alteration of Soil Carbon Pools and Communities of Mycorrhizal Fungi in Chaparral Exposed to Elevated Carbon Dioxide

We examined the effects of atmospheric carbon dioxide (CO₂) enrichment on belowground carbon (C) pools and arbuscular mycorrhizal (AM) fungi in a chaparral community in southern California. Chambers enclosing intact mesocosms dominated by Adenostoma fasciculatum were exposed for 3.5 years to CO₂ levels ranging from 250 to 750 ppm. Pools of total C in bulk soil and in water-stable aggregates (WSA) increased 1.5- and threefold, respectively, between the 250- and 650-ppm treatments. In addition, the abundance of live AM hyphae and spores rose markedly over the same range of CO₂, and the community composition shifted toward dominance by the AM genera Scutellospora and Acaulospora. Net ecosystem exchange of C with the atmosphere declined with CO₂ treatment. It appears that under CO₂ enrichment, extra C was added to the soil via AM fungi. Moreover, AM fungi were predominant in WSA and may shunt C into these aggregates versus bulk soil. Alternatively, C may be retained longer within WSA than within bulk soil. We note that differences between the soil fractions may act as a potential feedback on C cycling between the soil and atmosphere.     

Long-term responses of boreal vegetation to global change: an experimental and modelling investigation

The response of boreal ecosystems to future global change is an uncertain but potentially critical component of the feedback between the terrestrial biosphere and the atmosphere. To reduce some of the uncertainties in predicting the responses of this key ecosystem, the climate change experiment (CLIMEX) exposed an entire undisturbed catchment of boreal vegetation to CO₂ enrichment (560 ppmv) and climate change (+ 5 °C in winter, + 3 °C in summer) for three years (1994–96). This paper describes the leaf metabolic responses of the vegetation to the experimental treatment and model simulations of possible future changes in the hydrological and carbon balance of the site. Randomized intervention analysis of the leaf gas exchange measurements for the dominant species indicated Pinus sylvestris had significantly (P < 0.01) higher photosynthetic rates and Betula pubescens and Vaccinium myrtillus had significantly (P < 0.01) lower stomatal conductances after three years treatment compared to the controls. These responses led to sustained increases in leaf water-use efficiency of all species of trees and ground shrubs, as determined from carbon isotope analyses. Photosynthesis (A) vs. intercellular CO₂ (c_i) response curves (A/c_i responses), RuBisCo analysis and leaf nitrogen data together suggested none of the species investigated exhibited down-regulation in photosynthetic capacity. At the whole ecosystem level, the improved water economy of the plants did not translate into increased catchment runoff. Modelling simulations for the site indicate this was most likely brought about by a compensatory increase in evapotranspiration. In terms of the carbon budget of the site, the ecosystem model indicates that increased CO₂ and temperature would lead to boreal ecosystems of the type used in CLIMEX, and typical of much of southern Norway, acting as moderate net sinks for CO₂.     

Ecosystem responses to water and nitrogen amendment in a California grassland

The world's ecosystems are experiencing simultaneous changes in the supply of multiple limiting resources. Two of these, water and nitrogen (N) can strongly limit grassland production and can affect community composition and biogeochemical cycles in different ways. Grassland ecosystems in California may be particularly vulnerable to current and predicted changes in precipitation and N deposition, and ecosystem responses to potential interactive effects of water and N are not well understood. Here, we show strong colimitation of plant production resulting from factorial addition of water and N. In addition, water and N addition in combination led to increased dominance of the two most abundant grass species, while N addition regardless of water availability led to decreased species diversity. Late season carbon (C) flux response to water addition depended on N. Only plots that received additional water, but not N, still showed net ecosystem C uptake at the end of the experiment. Our results suggest that grassland ecosystem response to N deposition will be strongly dependent on future precipitation patterns.     

Climate change effects on plant biomass alter dominance patterns and community evenness in an experimental old‐field ecosystem

Atmospheric and climatic change can alter plant biomass production and plant community composition. However, we know little about how climate change‐induced alterations in biomass production affect plant species composition. To better understand how climate change will alter both individual plant species and community biomass, we manipulated atmospheric [CO₂], air temperature, and precipitation in a constructed old‐field ecosystem. Specifically, we compared the responses of dominant and subdominant species to our climatic treatments, and explored how changes in plant dominance patterns alter community evenness over 2 years. Our study resulted in four major findings: (1) all treatments, elevated [CO₂], warming, and increased precipitation increased plant community biomass and the effects were additive rather than interactive, (2) plant species differed in their response to the treatments, resulting in shifts in the proportional biomass of individual species, which altered the plant community composition; however, the plant community response was largely driven by the positive precipitation response of Lespedeza, the most dominant species in the community, (3) precipitation explained most of the variation in plant community composition among treatments, and (4) changes in precipitation caused a shift in the dominant species proportional biomass that resulted in lower community evenness in the wet relative to dry treatments. Interestingly, compositional and evenness responses of the subdominant community to the treatments did not always follow the responses of the whole plant community. Our data suggest that changes in plant dominance patterns and community evenness are an important part of community responses to climatic change, and generally, that such compositional shifts can alter ecosystem biomass production and nutrient inputs.     

Linking microbial activity and soil organic matter transformations in forest soils under elevated CO2

Soil organic matter (SOM) dynamics ultimately govern the ability of soil to provide long‐term C sequestration and the nutrients required for ecosystem productivity. Predicting belowground responses to elevated CO₂ requires an integrated understanding of SOM transformations and the microbial activity that governs them. It remains unclear how the microorganisms upon which these transformations depend will function in an elevated CO₂ world. This study examines SOM transformations and microbial metabolism in soils from the Duke Free Air Carbon Enrichment site in North Carolina, USA. We assessed microbial respiration and net nitrogen (N) mineralization in soils with and without elevated CO₂ exposure during a 100‐day incubation. We also traced the depleted C isotopic signature of the supplemental CO₂ into SOM and the soils' phospholipid fatty acids (PLFA), which serve as biomarkers for living cells. Cumulative net N mineralization in elevated CO₂ soils was 50% that in control soils after a 100‐day incubation. Respiration was not altered with elevated CO₂. C : N ratios of bulk SOM did not change with elevated CO₂, but incubation data suggest that the C : N ratios of mineralized organic matter increased with elevated CO₂. Values of SOM δ¹³C were depleted with elevated CO₂ (?26.7±0.2 vs. ?30.2±0.3‰), reflecting the depleted signature of the supplemental CO₂. We compared δ¹³C of individual PLFA with the δ¹³C of SOM to discern incorporation of the depleted C isotopic signature into soil microbial groups in elevated CO₂ plots. PLFA i15:0, a15:0, and 10Met18:0 reflected significant incorporation of recently produced photosynthate, suggesting that the bacterial groups defined by these biomarkers are active metabolizers in elevated CO₂ soils. At least one of these groups (actinomycetes, 10Met18:0) specializes in metabolizing less labile substrates. Because control plots did not receive an equivalent ¹³C tracer, we cannot determine from these data whether this group of organisms was stimulated by elevated CO₂ compared with these organisms in control soils. Stimulation of this group, if it occurred in the elevated CO₂ plot, would be consistent with a decline in the availability of mineralizable organic matter with elevated CO₂, which incubation data suggest may be the case in these soils.     

Plant community responses to nitrogen addition and increased precipitation: the importance of water availability and species traits

Global nitrogen (N) enrichment and changing precipitation regimes are likely to alter plant community structure and composition, with consequent influences on biodiversity and ecosystem functioning. Responses of plant community structure and composition to N addition and increased precipitation were examined in a temperate steppe in northern China. Increased precipitation and N addition stimulated and suppressed community species richness, respectively, across 6 years (2005–2010) of the manipulative experiment. N addition and increased precipitation significantly altered plant community structure and composition at functional groups levels. The significant relationship between species richness and soil moisture (SM) suggests that plant community structure is mediated by water under changing environmental conditions. In addition, plant height played an important role in affecting the responses of plant communities to N addition, and the effects of increased precipitation on plant community were dependent on species rooting depth. Our results highlight the importance and complexity of both abiotic (SM) and biotic factors (species traits) in structuring plant community under changing environmental scenarios. These findings indicate that knowledge of species traits can contribute to mechanistic understanding and projection of vegetation dynamics in response to future environmental change.     

Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization

The extramatrical mycelia (EMM) of ectomycorrhizal fungi make up a large proportion of the microbial diversity and biomass in temperate forest soils. Thus, their response to elevated CO(2) can have large effects on plant nutrient acquisition and carbon movement through forests. Here, the effects of CO(2) and nitrogen (N) fertilization on EMM biomass and community structure in Pinus taeda forest plots were examined using sand-filled mesh bags buried in the field, the contents of which were analyzed by phospholipid fatty acid (PLFA) and DNA sequencing. A total of 2138 sequences comprising 295 taxa were recovered; most (83.5%) were from ectomycorrhizal fungal taxa. No biomass increase was detected in elevated CO(2) plots relative to control plots, but individual taxa responded to both CO(2) and N fertilization, four of the six most abundant taxa were less frequent in N-fertilized plots. Thelephoroid and athelioid taxa were both frequent and abundant as EMM, and thelephoroid richness was extremely high. Russula and Cortinariaceae taxa were less abundant and boletoid taxa were more abundant as EMM relative to ectomycorrhizas. The EMM community, sampled across seasons and years, was dynamic with a high degree of interspecific variation in response to CO(2) enrichment and N fertilization.     

Using an ecosystem model linked to GCM-derived local weather scenarios to analyse effects of climate change and elevated CO2 on dry matter production and partitioning, and water use in temperate managed grasslands

Local effects of climate change (CC) and elevated CO₂ (2 × CO₂, 660 μmol mol^–1) on managed temperate grasslands were assessed by forcing a dynamic ecosystem model with weather scenarios. The aims of the study were to compare the relative importance of individual and combined effects of CC, 2 × CO₂, and photosynthetic acclimation, and to assess the importance of local site conditions. The model was driven by hourly means for temperature (T), precipitation (P), global radiation (G), vapour pressure (VP), and wind speed (U). Local climate scenarios were derived by statistical downscaling techniques from a 2 × CO₂ simulation with the General Circulation Model of the Canadian Climate Centre (CCC-GCMII). Simulations over 14 growing seasons to account for year-to-year variability of climate were carried out for a low, relatively dry site, and a high, more humid site. At both sites, shoot dry matter responded positively to 2 × CO₂ with the site at low elevation being more sensitive than the higher site. The effect of assumed changes in climate was negative at the lower, but positive at the higher site. Shoot dry matter was more sensitive to the effects of 2 × CO₂ than to CC. Both effects combined increased shoot dry matter by up to 20%. This was attributed to direct effects of 2 × CO₂ and increased T, and indirect stimulation via increased soil N availability. Biomass partitioning to roots increased with 2 × CO₂ but decreased with CC, while an intermediate response resulted from the combination. Leaf area index (LAI) increased under 2 × CO₂, but not enough to compensate fully for a decrease in leaf conductance. Under the 2 × CO₂ scenario evapotranspiration (ET) decreased, but increased under CC. Photosynthetic acclimation reduced the effect of 2 × CO₂ on shoot growth, but had little effect on ET. The seasonal water use efficiency (WUE) was improved under 2 × CO₂, and reduced under CC. With the combination of both factors, the change was small but still positive, especially at the high elevation site with more favourable soil water conditions. This reflects the stronger positive yield response in combination with a smaller increase in ET under cooler, more humid conditions. The results for the combination of factors suggest that except for shoot growth, effects of 2 × CO₂ and CC tend to offset each other. While CC determines the sign of the ET response, the sign of the biomass response is determined by 2 × CO₂. The results highlight the importance of a site-specific analysis of ecosystem responses by using a flexible approach based on a combination of state-of-the-art downscaling, spatially resolved data sets, and a mechanistic model to obtain quantitative and reproducible assessments of climate change impacts at the ecosystem level.     

Negative feedback on a perennial crop: Fusarium crown and root rot of asparagus is related to changes in soil microbial community structure

The dynamic equilibrium of an ecosystem is driven by mutual feedback interactions between plants and soil microorganisms. Asparagus exerts a particularly strong influence on its soil environment through abundant production of persistent phenolic acids, which impact selectively soil microorganisms and may be involved in Fusarium crown and root rot (FCRR) of asparagus. In a survey of 50 asparagus plantations of the province of Québec, we found that FCRR was associated with a profound cultivar-specific, reorganization of the soil microbial community, as revealed by phospholipid fatty acid (PLFA) profiling. According to PLFA indicators, microbial biodiversity as well as bacterial and fungal abundance dropped sharply with the onset of FCRR in fields planted with the cultivar Guelph Millenium. This drop was followed by a similar drop in the arbuscular mycorrhizal population. Biodiversity and microbial population size then increased to finally reach a new equilibrium. Discriminant analysis of PLFA profiles obtained from soil samples also indicated a shift in soil microbial community structure associated with FCRR development in fields planted with the cultivar Jersey Giant. Different soil biological conditions, as indicated by microbial biomass C and N and soil enzyme activities, were associated with different cultivars. Preceding crop, manure application, geographical location and tillage depth also influenced the structure of soil microbial communities in asparagus plantations, as determined by PLFA profiling. If higher FCRR incidence is a consequence of the soil microbial community reorganization, means to reduce FCRR incidence in asparagus plantations may be found among practices such as soil organic fertilization, soil tillage and intercropping strategies that would dilute the negative influence of asparagus on the soil microbial community. Finally, FCRR outbreaks were generally promoted by a previous crop of maize. It seems that maize and asparagus host a F. proliferatum teleomorph (Gibberella fujikoroi) of the same mating type.     

Soil nutrient heterogeneity interacts with elevated CO2 and nutrient availability to determine species and assemblage responses in a model grassland community

Interactive effects of atmospheric CO(2) concentration ([CO(2)]), soil nutrient availability and soil nutrient spatial distribution on the structure and function of plant assemblages remain largely unexplored. Here we conducted a microcosm experiment to evaluate these interactions using a grassland assemblage formed by Lolium perenne, Plantago lanceolata, Trifolium repens, Anthoxanthum odoratum and Holcus lanatus. Assemblages exhibited precise root foraging patterns, had higher total and below-ground biomass, and captured more nitrogen when nutrients were supplied heterogeneously. Root foraging responses were modified by nutrient availability, and the patterns of N capture by interactions between nutrient distribution, availability and [CO(2)]. Greater above-ground biomass was observed under elevated CO(2) only under homogeneous conditions of nutrient supply and at the highest availability level. CO(2) interacted with nutrient distribution and availability to determine foliar percentage N and below : above-ground biomass ratios, respectively. Interactions between nutrient distribution and CO(2) determined the relative contribution to above-ground biomass of four of the species. The responses of dominant and subordinate species to [CO(2)] were dependent on the availability and distribution of nutrients. Our results suggest that soil nutrient distribution has the potential to influence the response of plant species and assemblages to changes in [CO(2)] and nutrient availability.     

Temperate forest responses to carbon dioxide, temperature and nitrogen: a model analysis

The ITE Edinburgh Forest Model, which describes diurnal and seasonal changes in the pools and fluxes of C, N and water in a fully coupled forest–soil system, was parametrized to simulate a managed conifer plantation in upland Britain. The model was used to examine (i) the transient effects on forest growth of an IS92a scenario of increasing [CO₂] and temperature over two future rotations, and (ii) the equilibrium (sustainable) effects of all combinations of increases in [CO₂] from 350 to 550 and 750 μmol mol^?1, mean annual temperature from 7.5 to 8.5 and 9.5°C and annual inputs of 20 or 40 kg N ha^?1. Changes in underlying processes represented in the model were then used to explain the responses. Eight conclusions were supported by the model for this forest type and climate.

• 1 Increasing temperatures above 3°C alone may cause forest decline owing to water stress.
• 2 Elevated [CO₂] can protect trees from water stress that they may otherwise suffer in response to increased temperature.
• 3 In N-limiting conditions, elevated [CO₂] can increase allocation to roots with little increase in leaf area, whereas in N-rich conditions elevated [CO₂] may not increase allocation to roots and generally increases leaf area.
• 4 Elevated [CO₂] can decrease water use by forests in N-limited conditions and increase water use in N-rich conditions.
• 5 Elevated [CO₂] can increase forest productivity even in N-limiting conditions owing to increased N acquisition and use efficiency.
• 6 Rising temperatures (along with rising [CO₂]) may increase or decrease forest productivity depending on the supply of N and changes in water stress.
• 7 Gaseous losses of N from the soil can increase or decrease in response to elevated [CO₂] and temperature.
• 8 Projected increases in [CO₂] and temperature (IS92a) are likely to increase net ecosystem productivity and hence C sequestration in temperate forests.