Theory and experiments suggest that rhizodeposition can accelerate N-cycling by stimulating microbial decomposition of soil organic matter (SOM). However, there are remarkably few experimental ...demonstrations on the degree to which variations in root exudation alter rhizosphere N dynamics in the field. We conducted a series of in situ substrate addition experiments and a modeling exercise to investigate how exudate mimics and enzyme solutions (at varying concentrations) influence rhizosphere SOM and N dynamics in a loblolly pine (Pinus taeda) plantation (Duke Forest). Exudates were added semi-continuously to unfertilized and fertilized soils in summer and fall; enzymes were added during the following summer. Exudate additions enhanced the microbial biomass specific activities of enzymes that degrade fast-cycling N pools (i.e., amino acids and amino sugars), and increased microbial allocation to N-degrading compounds. More, such effects occurred at low exudate concentrations in unfertilized soil and at higher concentrations in fertilized soil. Direct additions of a subset of enzymes (amino sugar- and cellulose-degrading) to soils increased net N mineralization rates, but additions of enzymes that cleave slow-cycling SOM did not. We conclude that exudates can stimulate microbes to decompose labile SOM and release N without concomitant changes in microbial biomass, yet the investment of plants to trigger this effect may be greater in N-rich soils.
•Evidence for a mechanistic link between root exudation and accelerated N cycling.•Exudate additions enhanced fast-cycling N degrading enzyme activities.•Additions of fast-cycling N degrading enzymes increased net N mineralization.•Much of the extra N is likely derived from amino acids and amino sugars.•Investment of plants to trigger SOM decomposition is much higher in N-rich soils.
Abstract
Even though the two dominant mycorrhizal associations of temperate tree species differentially couple carbon (C) and nitrogen (N) cycles in temperate forests, systematic differences between ...the biogeochemical cycles of arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) tree species remain poorly described. A classification according to the mycorrhizal type offers the chance, though, to develop a global frame concept for the prediction of temperate ecosystem responses to environmental change. Focusing on the influence of mycorrhizal types on two key plant processes of biogeochemical cycling (root exudation and N acquisition), we investigated four temperate deciduous tree species per mycorrhizal type in a drought experiment in large mesocosms. We hypothesized that (H1) C loss by root exudation is higher in ECM than in AM trees, (H2) drought leads to higher reductions in root exudation of drought-sensitive ECM trees and (H3) inorganic N uptake is higher in AM than in ECM trees. In contradiction to H2, we found no systematic difference in root exudation between the mycorrhizal types at ample soil moisture, but almost twofold higher exudation in ECM trees when exposed to soil drought. In addition, photosynthetic C cost of root exudation strongly increased by ~10-fold in drought-treated ECM trees, while it only doubled in AM trees, which confirms H1. With respect to H3, we corroborated that AM trees had higher absolute and relative inorganic N acquisition rates than ECM trees, while the organic N uptake did not differ between mycorrhizal types. We conclude that ECM trees are less efficient in inorganic N uptake than AM trees, but ECM trees increase root C release as an adaptive response to dry soil to maintain hydraulic conductivity and/or nutrient availability. These systematic differences in key biogeochemical processes support hints on the key role of the mycorrhizal types in coupling C and N cycles in temperate forests.
Global vegetation models use conceived relationships between functional traits to simulate ecosystem responses to environmental change. In this context, the concept of the leaf economics spectrum ...(LES) suggests coordinated leaf trait variation, and separates species which invest resources into short-lived leaves with a high expected energy return rate from species with longer-lived leaves and slower energy return. While it has been assumed that being fast (acquisitive) or slow (conservative) is a general feature for all organ systems, the translation of the LES into a root economics spectrum (RES) for tree species has been hitherto inconclusive. This may be partly due to the assumption that the bulk of tree fine roots have similar uptake functions as leaves, despite the heterogeneity of their environments and resources. In this study we investigated well-established functional leaf and stature traits as well as a high number of fine root traits (14 traits split by different root orders) of 13 dominant or subdominant temperate tree species of Central Europe, representing two phylogenetic groups (gymnosperms and angiosperms) and two mycorrhizal associations (arbuscular and ectomycorrhizal). We found reflected variation in leaf and lower-order root traits in some (surface areas and C:N) but not all (N content and longevity) traits central to the LES. Accordingly, the LES was not mirrored belowground. We identified significant phylogenetic signal in morphological lower-order root traits, i.e., in root tissue density, root diameter, and specific root length. By contrast, root architecture (root branching) was influenced by the mycorrhizal association type which developed independent from phylogeny of the host tree. In structural equation models we show that root branching significantly influences both belowground (direct influence on root C:N) and aboveground (indirect influences on specific leaf area and leaf longevity) traits which relate to resource investment and lifespan. We conclude that branching of lower order roots can be considered a leading root trait of the plant economics spectrum of temperate trees, since it relates to the mycorrhizal association type and belowground resource exploitation; while the dominance of the phylogenetic signal over environmental filtering makes morphological root traits less central for tree economics spectra across different environments.
Root exudation is a key plant function with a large influence on soil organic matter dynamics and plant–soil feedbacks in forest ecosystems. Yet despite its importance, the main ecological drivers of ...root exudation in mature forest trees remain to be identified.
During two growing seasons, we analyzed the dependence of in situ collected root exudates on root morphology, soil chemistry and nutrient availability in six mature European beech (Fagus sylvatica L.) forests on a broad range of bedrock types.
Root morphology was a major driver of root exudation across the nutrient availability gradient. A doubling of specific root length exponentially increased exudation rates of mature trees by c. 5-fold. Root exudation was also closely negatively related to soil pH and nitrogen (N) availability. At acidic and N-poor sites, where fungal biomass was reduced, exudation rates were c. 3-fold higher than at N- and base-richer sites and correlated negatively with the activity of enzymes degrading less bioavailable carbon (C) and N in the bulk soil.
We conclude that root exudation increases on highly acidic, N-poor soils, in which fungal activity is reduced and a greater portion of the assimilated plant C is shifted to the external ecosystem C cycle.
How tree root systems will respond to increased drought stress, as predicted for parts of Central Europe, is not well understood. According to the optimal partitioning theory, plants should enhance ...root growth relative to aboveground growth in order to reduce water limitations. We tested this prediction in a transect study with 14 mature forest stands of European beech (Fagus sylvatica L.) by analysing the response of the fine root system to a large decrease in annual precipitation (970-520 mm yr⁻¹). In 3 years with contrasting precipitation regimes, we investigated leaf area and leaf biomass, fine root biomass and necromass (organic layer and mineral soil to 40 cm) and fine root productivity (ingrowth core approach), and analysed the dependence on precipitation, temperature, soil nutrient availability and stand structure. In contrast to the optimal partitioning theory, fine root biomass decreased by about a third from stands with >950 mm yr⁻¹ to those with <550 mm yr⁻¹, while leaf biomass remained constant, resulting in a significant decrease, and not an increase, in the fine root/leaf biomass ratio towards drier sites. Average fine root diameter decreased towards the drier stands, thereby partly compensating for the loss in root biomass and surface area. Both δ¹³C-signature of fine root mass and the ingrowth core data indicated a higher fine root turnover in the drier stands. Principal components analyses (PCA) and regression analyses revealed a positive influence of precipitation on the profile total of fine root biomass in the 14 stands and a negative one of temperature and plant-available soil phosphorus. We hypothesize that summer droughts lead to increased fine root mortality, thereby reducing root biomass, but they also stimulate compensatory fine root production in the drier stands. We conclude that the optimal partitioning theory fails to explain the observed decrease in the fine root/leaf biomass ratio, but is supported by the data if carbon allocation to roots is considered, which would account for enhanced root turnover in drier environments.
Plant growth is usually constrained by the availability of nutrients, water, or temperature, rather than photosynthetic carbon (C) fixation. Under these conditions leaf growth is curtailed more than ...C fixation, and the surplus photosynthates are exported from the leaf. In plants limited by nitrogen (N) or phosphorus (P), photosynthates are converted into sugars and secondary metabolites. Some surplus C is translocated to roots and released as root exudates or transferred to root-associated microorganisms. Surplus C is also produced under low moisture availability, low temperature, and high atmospheric CO2 concentrations, with similar below-ground effects. Many interactions among above- and below-ground ecosystem components can be parsimoniously explained by the production, distribution, and release of surplus C under conditions that limit plant growth.
Plant growth is normally constrained by nutrients, water or temperature, not photosynthesis, and plants often have surplus carbohydrates.Secondary metabolites are produced in N-limited plants primarily to dispose of surplus carbon, although they may subsequently help reduce browsing damage.Surplus carbohydrates are translocated from leaves and below ground some are discharged via exudates and mycorrhizal fungi.Root exudates contain more of the elements that plants have in surplus, and less of those in short supply.The abundance and type of mycorrhizal fungi is influenced by the amount and composition of surplus carbon in roots.Surplus carbon provides an alternative lens though which to view interactions between plants and soil organisms.
Increases in summer droughts and nitrogen (N) deposition have raised concerns of widespread biodiversity loss and nutrient imbalances, but our understanding of the ecological role of ectomycorrhizal ...fungal (ECMF) diversity in mediating root functions remains a major knowledge gap.
We used different global change scenarios to experimentally alter the composition of ECMF communities colonizing European beech saplings and examined the consequences for phosphorus (P) uptake (H3
33PO4 feeding experiment) and use efficiencies of trees. Specifically, we simulated increases in temperature and N deposition and decreases in soil moisture and P availability in a factorial experiment.
Here, we show that ECMF α diversity is a major factor contributing to root functioning under global change. P uptake efficiency of beech significantly increased with increasing ECMF species richness and diversity, as well as with decreasing P availability. As a consequence of decreases in ECMF diversity, P uptake efficiency decreased when soil moisture was limiting. By contrast, P use efficiencies were a direct (negative) function of P availability and not of ECMF diversity.
We conclude that increasing summer droughts may reduce ECMF diversity and the complementarity of P uptake by ECMF species, which will add to negative growth effects expected from nutrient imbalances under global change.
A common finding in multiple CO2 enrichment experiments in forests is the lack of soil carbon (C) accumulation owing to microbial priming of ‘old’ soil organic matter (SOM). However, soil C losses ...may also result from the accelerated turnover of ‘young’ microbial tissues that are rich in nitrogen (N) relative to bulk SOM. We measured root‐induced changes in soil C dynamics in a pine forest exposed to elevated CO2 and N enrichment by combining stable isotope analyses, molecular characterisations of SOM and microbial assays. We find strong evidence that the accelerated turnover of root‐derived C under elevated CO2 is sufficient in magnitude to offset increased belowground inputs. In addition, the C losses were associated with accelerated N cycling, suggesting that trees exposed to elevated CO2 not only enhance N availability by stimulating microbial decomposition of SOM via priming but also increase the rate at which N cycles through microbial pools.
Temperate forests have recently been identified as being continuing sinks for carbon even in their mature and senescent stages. However, modeling exercises indicate that a warmer and drier climate as ...predicted for parts of Central Europe may substantially alter the source/sink function of these economically important ecosystems. In a transect study with 14 mature European beech (Fagus sylvatica L.) forests growing on uniform geological substrate, we analyzed the influence of a large reduction of annual precipitation (970-520 mm yr⁻¹) on the carbon stocks in fast and slow pools, independent of the well-known aging effect. We investigated the C storage in the organic L, F, H layers, the mineral soil to 100 cm, and in the biomass (stem, leaves, fine roots), and analyzed the dependence of these pools on precipitation. Soil organic carbon decreased by about 25% from stands with > 900 mm yr⁻¹ to those with < 600 mm yr⁻¹; while the carbon storage in beech stems slightly increased. Reduced precipitation affected the biomass C pool in particular in the fine root fraction but much less in the leaf biomass and stem fractions. Fine root turnover increased with a precipitation reduction, even though stand fine root biomass and SOC in the organic L, F, and H layers decreased. According to regression analyses, the C storage in the organic layers was mainly controlled by the size of the fine root C pool suggesting an important role of fine root turnover for the C transfer from tree biomass to the SOC pool. We conclude that the long-term consequence of a substantial precipitation decrease would be a reduction of the mineral soil and organic layer SOC pools, mainly due to higher decomposition rates. This could turn temperate beech forests into significant carbon sources instead of sinks under global warming.
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