Informing climate models with rapid chamber measurements of forest carbon uptake.

Models predicting ecosystem carbon dioxide (CO2 ) exchange under future climate change rely on relatively few real-world tests of their assumptions and outputs. Here, we demonstrate a rapid and cost-effective method to estimate CO2 exchange from intact vegetation patches under varying atmospheric CO2 concentrations. We find that net ecosystem CO2 uptake (NEE) in a boreal forest rose linearly by 4.7 ± 0.2% of the current ambient rate for every 10 ppm CO2 increase, with no detectable influence of foliar biomass, season, or nitrogen (N) fertilization. The lack of any clear short-term NEE response to fertilization in such an N-limited system is inconsistent with the instantaneous downregulation of photosynthesis formalized in many global models. Incorporating an alternative mechanism with considerable empirical support - diversion of excess carbon to storage compounds - into an existing earth system model brings the model output into closer agreement with our field measurements. A global simulation incorporating this modified model reduces a long-standing mismatch between the modeled and observed seasonal amplitude of atmospheric CO2 . Wider application of this chamber approach would provide critical data needed to further improve modeled projections of biosphere-atmosphere CO2 exchange in a changing climate.

Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests?

Symbioses between plant roots and mycorrhizal fungi are thought to enhance plant uptake of nutrients through a favourable exchange for photosynthates. Ectomycorrhizal fungi are considered to play this vital role for trees in nitrogen (N)-limited boreal forests. We followed symbiotic carbon (C)-N exchange in a large-scale boreal pine forest experiment by tracing (13) CO(2) absorbed through tree photosynthesis and (15) N injected into a soil layer in which ectomycorrhizal fungi dominate the microbial community. We detected little (15) N in tree canopies, but high levels in soil microbes and in mycorrhizal root tips, illustrating effective soil N immobilization, especially in late summer, when tree belowground C allocation was high. Additions of N fertilizer to the soil before labelling shifted the incorporation of (15) N from soil microbes and root tips to tree foliage. These results were tested in a model for C-N exchange between trees and mycorrhizal fungi, suggesting that ectomycorrhizal fungi transfer small fractions of absorbed N to trees under N-limited conditions, but larger fractions if more N is available. We suggest that greater allocation of C from trees to ectomycorrhizal fungi increases N retention in soil mycelium, driving boreal forests towards more severe N limitation at low N supply.

Fruit production in three masting tree species does not rely on stored carbon reserves.

Fruiting is typically considered to massively burden the seasonal carbon budget of trees. The cost of reproduction has therefore been suggested as a proximate factor explaining observed mast-fruiting patterns. Here, we used a large-scale, continuous (13)C labeling of mature, deciduous trees in a temperate Swiss forest to investigate to what extent fruit formation in three species with masting reproduction behavior (Carpinus betulus, Fagus sylvatica, Quercus petraea) relies on the import of stored carbon reserves. Using a free-air CO2 enrichment system, we exposed trees to (13)C-depleted CO2 during 8 consecutive years. By the end of this experiment, carbon reserve pools had significantly lower δ(13)C values compared to control trees. δ(13)C analysis of new biomass during the first season after termination of the CO2 enrichment allowed us to distinguish the sources of built-in carbon (old carbon reserves vs. current assimilates). Flowers and expanding leaves carried a significant (13)C label from old carbon stores. In contrast, fruits and vegetative infructescence tissues were exclusively produced from current, unlabeled photoassimilates in all three species, including F. sylvatica, which had a strong masting season. Analyses of δ(13)C in purified starch from xylem of fruit-bearing shoots revealed a complete turn-over of starch during the season, likely due to its usage for bud break. This study is the first to directly demonstrate that fruiting is independent from old carbon reserves in masting trees, with significant implications for mechanistic models that explain mast seeding.

Allocation of carbon to fine root compounds and their residence times in a boreal forest depend on root size class and season.

Fine roots play a key role in the forest carbon balance, but their carbon dynamics remain largely unknown. We pulse labelled 50 m(2) patches of young boreal forest by exposure to (13)CO(2) in early and late summer. Labelled photosynthates were traced into carbon compounds of < 1 and 1-3 mm diameter roots (fine roots), and into bulk tissue of these and first-order roots (root tips). Root tips were the most strongly labelled size class. Carbon allocation to all size classes was higher in late than in early summer; mean residence times (MRTs) in starch increased from 4 to 11 months. In structural compounds, MRTs were 0.8 yr in tips and 1.8 yr in fine roots. The MRT of carbon in sugars was in the range of days. Functional differences within the fine root population were indicated by carbon allocation patterns and residence times. Pronounced allocation of recent carbon and higher turnover rates in tips are associated with their role in nutrient and water acquisition. In fine roots, longer MRTs but high allocation to sugars and starch reflect their role in structural support and storage. Accounting for heterogeneity in carbon residence times will improve and most probably reduce the estimates of fine root production.

Expanding leaves of mature deciduous forest trees rapidly become autotrophic.

Emerging leaves in evergreen tree species are supplied with carbon (C) from the previous year's foliage. In deciduous trees, no older leaves are present, and the early phase of leaf development must rely on C reserves from other tissues. How soon developing leaves become autotrophic and switch from being C sinks to sources has rarely been studied in mature forest trees, and simultaneous comparisons of species are scarce. Using a canopy crane and a simple (13)CO(2)-pulse-labelling technique, we demonstrate that young leaves of mature trees in three European deciduous species (Fagus sylvatica L., Quercus petraea (Matt.) Liebl., Tilia platyphyllos Scop.) start assimilating CO(2) at a very early stage of development (10-50% expanded). One month after labelling, all leaves were still strongly (13)C enriched, suggesting that recent photosynthates had been incorporated into slow turnover pools such as cellulose or lignin and thus had contributed to leaf growth. In line with previous studies performed at the same site, we found stronger incorporation of recent photosynthates into growing tissues of T. platyphyllos compared with F. sylvatica and Q. petraea. Non-structural carbohydrate (NSC) concentrations analysed for one of the three study species (F. sylvatica) showed that sugar and starch pools rapidly increased during leaf development, suggesting that newly developed leaves soon produce more NSC than can be used for growth. In conclusion, our findings indicate that expanding leaves of mature deciduous trees become C autonomous at an early stage of development despite the presence of vast amounts of mobile carbohydrate reserves.

Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest.

SUMMARY: *The flux of carbon from tree photosynthesis through roots to ectomycorrhizal (ECM) fungi and other soil organisms is assumed to vary with season and with edaphic factors such as nitrogen availability, but these effects have not been quantified directly in the field. *To address this deficiency, we conducted high temporal-resolution tracing of (13)C from canopy photosynthesis to different groups of soil organisms in a young boreal Pinus sylvestris forest. *There was a 500% higher below-ground allocation of plant C in the late (August) season compared with the early season (June). Labelled C was primarily found in fungal fatty acid biomarkers (and rarely in bacterial biomarkers), and in Collembola, but not in Acari and Enchytraeidae. The production of sporocarps of ECM fungi was totally dependent on allocation of recent photosynthate in the late season. There was no short-term (2 wk) effect of additions of N to the soil, but after 1 yr, there was a 60% reduction of below-ground C allocation to soil biota. *Thus, organisms in forest soils, and their roles in ecosystem functions, appear highly sensitive to plant physiological responses to two major aspects of global change: changes in seasonal weather patterns and N eutrophication.

Short-term dynamics of abiotic and biotic soil 13CO2 effluxes after in situ 13CO2 pulse labelling of a boreal pine forest.

Physical diffusion of isotopic tracers into and out of soil pores causes considerable uncertainty for the timing and magnitude of plant belowground allocation in pulse-labelling experiments. Here, we partitioned soil CO(2) isotopic fluxes into abiotic tracer flux (physical return), heterotrophic flux, and autotrophic flux contributions following (13)CO(2) labelling of a Swedish Pinus sylvestris forest. Soil CO(2) efflux and its isotopic composition from a combination of deep and surface soil collars was monitored using a field-deployed mass spectrometer. Additionally, (13)CO(2) within the soil profile was monitored. Physical (abiotic) efflux of (13)CO(2) from soil pore spaces was found to be significant for up to 48 h after pulse labelling, and equalled the amount of biotic label flux over 6 d. Measured and modelled changes in (13)CO(2) concentration throughout the soil profile corroborated these results. Tracer return via soil CO(2) efflux correlated significantly with the proximity of collars to trees, while daily amplitudes of total flux (including heterotrophic and autotrophic sources) showed surprising time shifts compared with heterotrophic fluxes. The results show for the first time the significance of the confounding influence of physical isotopic CO(2)-tracer return from the soil matrix, calling for the inclusion of meaningful control treatments in future pulse-chase experiments.

Rapid mixing between old and new C pools in the canopy of mature forest trees.

Stable C isotope signals in plant tissues became a key tool in explaining growth responses to the environment. The technique is based on the fundamental assumption that the isotopic composition of a given unit of tissue (e.g. a tree ring) reflects the specific C uptake conditions in the leaf at a given time. Beyond the methodological implications of any deviation from this assumption, it is of physiological interest whether new C is transferred directly from sources (a photosynthesizing leaf) to structural sinks (e.g. adjacent stem tissue), or inherently passes through existing (mobile) C pools, which may be of variable (older) age. Here, we explore the fate of (13)C-labelled photosynthates in the crowns of a 30-35 m tall, mixed forest using a canopy crane. In all nine study species labelled C reached woody tissue within 2-9 h after labelling. Four months later, very small signals were left in branch wood of Tilia suggesting that low mixing of new, labelled C with old C had taken place. In contrast, signals in Fagus and Quercus had increased, indicating more intense mixing. This species-specific mixing of new with old C pools is likely to mask year- or season-specific linkages between tree ring formation and climate and has considerable implications for climate reconstruction using stable isotopes as proxies for past climatic conditions.

Canopy CO2 enrichment permits tracing the fate of recently assimilated carbon in a mature deciduous forest.

How rapidly newly assimilated carbon (C) is invested into recalcitrant structures of forests, and how closely C pools and fluxes are tied to photosynthesis, is largely unknown. A crane and a purpose-built free-air CO2 enrichment (FACE) system permitted us to label the canopy of a mature deciduous forest with 13C-depleted CO2 for 4 yr and continuously trace the flow of recent C through the forest without disturbance. Potted C4 grasses in the canopy ('isometers') served as a reference for the C-isotope input signal. After four growing seasons, leaves were completely labelled, while newly formed wood (tree rings) still contained 9% old C. Distinct labels were found in fine roots (38%) and sporocarps of mycorrhizal fungi (62%). Soil particles attached to fine roots contained 9% new C, whereas no measurable signal was detected in bulk soil. Soil-air CO2 consisted of 35% new C, indicating that considerable amounts of assimilates were rapidly returned back to the atmosphere. These data illustrate a relatively slow dilution of old mobile C pools in trees, but a pronounced allocation of very recent assimilates to C pools of short residence times.

Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2.

Whether rising atmospheric carbon dioxide (CO2) concentrations will cause forests to grow faster and store more carbon is an open question. Using free air CO2 release in combination with a canopy crane, we found an immediate and sustained enhancement of carbon flux through 35-meter-tall temperate forest trees when exposed to elevated CO2. However, there was no overall stimulation in stem growth and leaf litter production after 4 years. Photosynthetic capacity was not reduced, leaf chemistry changes were minor, and tree species differed in their responses. Although growing vigorously, these trees did not accrete more biomass carbon in stems in response to elevated CO2, thus challenging projections of growth responses derived from tests with smaller trees.