Peter Högberg

Large-scale forest girdling shows that current photosynthesis drives soil respiration

The respiratory activities of plant roots, of their mycorrhizal fungi and of the free-living microbial heterotrophs (decomposers) in soils are significant components of the global carbon balance, but their relative contributions remain uncertain. To separate mycorrhizal root respiration from heterotrophic respiration in a boreal pine forest, we conducted a large-scale tree-girdling experiment, comprising 9 plots each containing about 120 trees. Tree-girdling involves stripping the stem bark to the depth of the current xylem at breast height terminating the supply of current photosynthates to roots and their mycorrhizal fungi without physically disturbing the delicate root–microbe–soil system. Here we report that girdling reduced soil respiration within 1–2 months by about 54% relative to respiration on ungirdled control plots, and that decreases of up to 37% were detected within 5 days. These values clearly show that the flux of current assimilates to roots is a key driver of soil respiration; they are conservative estimates of root respiration, however, because girdling increased the use of starch reserves in the roots. Our results indicate that models of soil respiration should incorporate measures of photosynthesis and of seasonal patterns of photosynthate allocation to roots.

Boreal forest plants take up organic nitrogen

Plant growth in the boreal forest, the largest terrestrial biome, is generally limited by the availability of nitrogen. The presumed cause of this limitation is slow mineralization of soil organic nitrogen,. Here we demonstrate, to our knowledge for the first time, the uptake of organic nitrogen in the field by the trees Pinus sylvestris and Picea abies, the dwarf shrub Vaccinium myrtillus and the grass Deschampsia flexuosa. These results show that these plants, irrespective of their different types of root–fungal associations (mycorrhiza), bypass nitrogen mineralization. A trace of the amino acid glycine, labelled with the stable isotopes 13C and 15N, was injected into the organic (mor) layer of an old successional boreal coniferous forest. Ratios of 13C:15N in the roots showed that at least 91, 64 and 42% of the nitrogen from the absorbed glycine was taken up in intact glycine by the dwarf shrub, the grass and the trees, respectively. Rates of glycine uptake were similar to those of 15N-ammonium. Our data indicate that organic nitrogen is important for these different plants, even when they are competing with each other and with non-symbiotic microorganisms. This has major implications for our understanding of the effects of nitrogen deposition, global warming and intensified forestry.

Ecosystem effects of biodiversity manipulations in European grasslands.

We present a multisite analysis of the relationship between plant diversity and ecosystem functioning within the European BIODEPTH network of plant-diversity manipulation experiments. We report results of the analysis of 11 variables addressing several aspects of key ecosystem processes like biomass production, resource use (space, light, and nitrogen), and decomposition, measured across three years in plots of varying plant species richness at eight different European grassland field sites. Differences among sites explained substantial and significant amounts of the variation of most of the ecosystem processes examined. However, against this background of geographic variation, all the aspects of plant diversity and composition we examined (i.e., both numbers and types of species and functional groups) produced significant, mostly positive impacts on ecosystem processes. Analyses using the additive partitioning method revealed that complementarity effects (greater net yields than predicted from monocultures due to resource partitioning, positive interactions, etc.) were stronger and more consistent than selection effects (the covariance between monoculture yield and change in yield in mixtures) caused by dominance of species with particular traits. In general, communities with a higher diversity of species and functional groups were more productive and utilized resources more completely by intercepting more light, taking up more nitrogen, and occupying more of the available space. Diversity had significant effects through both increased vegetation cover and greater nitrogen retention by plants when this resource was more abundant through N2 fixation by legumes. However, additional positive diversity effects remained even after controlling for differences in vegetation cover and for the presence of legumes in communities. Diversity effects were stronger on above- than belowground processes. In particular, clear diversity effects on decomposition were only observed at one of the eight sites. The ecosystem effects of plant diversity also varied between sites and years. In general, diversity effects were lowest in the first year and stronger later in the experiment, indicating that they were not transitional due to community establishment. These analyses of our complete ecosystem process data set largely reinforce our previous results, and those from comparable biodiversity experiments, and extend the generality of diversity–ecosystem functioning relationships to multiple sites, years, and processes.

Does atmospheric deposition of nitrogen threaten Swedish forests

Abstract The health and productivity of forests is fundamentally important to many societies, and the culture and economy of Sweden are intimately linked with Swedens forests. Are the health and productivity of Swedens forests at risk from too much nitrogen from acid deposition? We evaluated this question by posing a number of specific questions, and synthesized information from the extensive research in Sweden on N deposition, fertilization and forest growth. We addressed the questions: Have Swedish forest soils acidified in recent decades? Are Swedish forest saturated with N, or do they have an excess of N? Will excessive N lead to forest decline? Will liming or vitalisation fertilization improve forest nutrition and health? We examined the ideas behind these questions, the available evidence, and whether the evidence supported or refuted the ideas. Several studies have documented reductions in soil pH (measured in water) in Swedish forests over periods of several decades. This acidification has been accompanied by increases in ionic strength of soil solutions, reduced base saturation and increased soil organic matter. The importance of each of these acidifying processes has not been investigated directly, but evidence supports a substantial role for each mechanism in at least some cases. Current expectations about rates of mineral weathering are not consistent with the evidence; rates of weathering appear to be greater than expected, and to differ depending on tree species. Swedish forests are not saturated with N; only a few stands near the southwest coast (with the highest deposition rates) show leaching losses of N that rival N deposition rates. Across all regions of Sweden, inadequate supplies of N limit forest growth. Within each region, some stands fail to respond to N fertilization (or respond with a decrease in growth), which is common for other forest types in other countries. Stands that have received heavy fertilization with N may become responsive to further fertilization with phosphorus (P) or base cations, and fertilization with trace amounts of boron (B) may be important on some soils. No evidence supports any widespread responsiveness of the forests to fertilization with other elements unless N is also added. Vitalisation fertilization (with non-N nutrients) has not demonstrated substantial improvements in tree growth, although most experiments have focused on N-limited sites rather than N-excess sites. Liming studies from Sweden and around Scandinavia indicate that forest health typically suffers after liming, including growth losses of 5 to 10% lasting one or more decades. The forests of Sweden averaged about 30% greater growth per hectare in the 1990s than in the 1950s, and extensive forest inventories show no indication of abnormal forest declines within this overall picture of improving growth. Hypotheses of declining forest growth as a function of the ratio of base cations to aluminum in soil solution can be tested with N fertilization experiments. The cation ratios uniformly declined with N fertilization, but growth typically increased, refuting the idea that cation ratios can represent changes in forest productivity. We conclude that no evidence supports the hypothesis of past or current deposition of N has reduced the health or productivity of Swedens forests; the opposite may have occurred. We also stress that several important questions cannot be addressed satisfactorily with current information. In particular, we recommend additional research on sites where N leaching rivals N deposition, elucidating mechanisms controlling N leaching and responses of trees to excessive levels of soil N.

15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils

Abstract15N natural abundances of soil total N, roots and mycorrhizas were studied in surface soil profiles in coniferous and broadleaved forests along a transect from central to northern Europe. Under conditions of N limitation in Sweden, there was an increase in δ15N of soil total N of up to 9% from the uppermost horizon of the organic mor layer down to the upper 0–5 cm of the mineral soil. The δ15N of roots was only slightly lower than that of soil total N in the upper organic horizon, but further down roots were up to 5% depleted under such conditions. In experimentally N-enriched forest in Sweden, i.e. in plots which have received an average of c. 100 kg N ha−1 year−1 for 20 years and which retain less than 50% of this added N in the stand and the soil down to 20 cm depth, and in some forests in central Europe, the increase in δ15N with depth in soil total N was smaller. An increase in δ15N of the surface soil was even observed on experimentally N-enriched plots, although other data suggest that the N fertilizer added was depleted in15N. In such cases roots could be enriched in15N relative to soil total N, suggesting that labelling of the surface soil is via the pathway: — available pools of N-plant N-litter N. Under N-limiting conditions roots of different species sampled from the same soil horizon showed similar δ15N. By contrast, in experimentally N-enriched forest δ15N of roots increased in the sequence: ericaceous dwarf shrubs<Scots pine<grass, suggesting increasing use of inorganic N along the sequence. Complementary studies at the major transect sites had shown that 90–99% of fine tree roots had ectomycorrhizas (ECMs). ECMs were 2% more enriched than corresponding non-mycorrhizal fine roots. Fungal sheaths stripped off ECMs were 2.4–6.4 enriched relative to the remaining root core. It is suggested that a flux of N through ECMs to aboveground parts in N-limited forests would leave 15N enriched compounds in fungal material, which could contribute to explain the observed δ15N profiles if fungal material is enriched, because it is a precursor of stable organic matter and recalcitrant N. This could act in addition to the previous explanation of the isotopically lighter soil surface in forests: plant uptake of 15N-depleted N and its redeposition onto the soil surface by litter-fall.

UPTAKE OF ORGANIC NITROGEN IN THE FIELD BY FOUR AGRICULTURALLY IMPORTANT PLANT SPECIES

Uptake of glycine was studied in four plants commonly used in grasslands in northern Europe (Phleum pratense, Trifolium hybridum, T. pratense, and Ranunculus acris) and compared to uptake of ammonium and nitrate. The experiment was conducted in the field, but with plants transferred to pots with soil 8–10 d before the start of the experiment. Plant uptake of U-13C215N glycine, 15NH4+, and 15NO3− was studied by injecting dilute (1 mmol/L) solutions of respectively labeled N source into the pots and harvesting plants 21 h later. Measurements of 13C and 15N in roots showed that, in all plants, part of the glycine N was taken up in the form of intact amino acid. Hence, regressions of plots of excess 13C against excess 15N showed that a minimum of 19–23% of the glycine-derived N was taken up as intact amino acid; possible losses of labeled C atoms of glycine during its metabolism in the plants implies that these estimates are conservative. Uptake of the different N sources was similar in the two Trifolium spec...

A synthesis: The role of nutrients as constraints on carbon balances in boreal and arctic regions

As in many ecosystems, carbon (C) cycling in arctic and boreal regions is tightly linked to the cycling of nutrients: nutrients (particularly nitrogen) are mineralized through the process of organic matter decomposition (C mineralization), and nutrient availability strongly constrains ecosystem C gain through primary production. This link between C and nutrient cycles has implications for how northern systems will respond to future climate warming and whether feedbacks to rising concentrations of atmospheric CO2 from these regions will be positive or negative. Warming is expected to cause a substantial release of C to the atmosphere because of increased decomposition of the large amounts of organic C present in high-latitude soils (a positive feedback to climate warming). However, increased nutrient mineralization associated with this decomposition is expected to stimulate primary production and ecosystem C gain, offsetting or even exceeding C lost through decomposition (a negative feedback to climate warming). Increased primary production with warming is consistent with results of numerous experiments showing increased plant growth with nutrient enrichment. Here we examine key assumptions behind this scenario: (1) temperature is a primary control of decomposition in northern regions, (2) increased decomposition and associated nutrient release are tightly coupled to plant nutrient uptake, and (3) short-term manipulations of temperature and nutrient availability accurately predict long-term responses to climate change.

SOIL CHEMISTRY AND PLANTS IN FENNOSCANDIAN BOREAL FOREST AS EXEMPLIFIED BY A LOCAL GRADIENT

In Fennoscandian boreal forests, in which productivity in general is N lim- ited, there are regular, topographically related variations in forest productivity and plant community composition. Regional surveys have demonstrated strong correlations among soil pH, N content, and base saturation on the one hand and plant productivity and com- munity composition on the other, but the nature of these relationships is poorly understood. We studied in detail the variation in and controls of soil acidity, availability of N and P, and changes in community composition and plant nutrition along a short (only 90 m long) but extreme forest productivity gradient in northern Sweden, which ranged from a ground- water recharge area with low productivity to a very productive discharge area. The pH in the soil solution of the mor layer ranged from 3.5 in the recharge area to 6.4 in the discharge area, and it was strongly correlated with the base saturation of the exchange complex. Neither the acid strength of organic matter, the ionic strength of the soil solution, nor the quantity of acids could explain more than a minor part of this variation in pH. There were strong correlations between total N in the mor layer and soil solution pH (r = 0.97) and base saturation of the exchange complex (r = 0.88). At the poor end of the transect the concentration of inorganic N was very low in the mor, and plants with either ectomycorrhizae (ECM) or ericoid mycorrhizae (EM) dominated. With increasing pH, there was an increase in NH4 concentrations, while plants that potentially have arbus- cular mycorrhizae (AM) became prominent along with ECM and EM species. In the dis- charge area, which comprised only the last 10 m of the transect, NO3 dominated over NH4 in the soil solution, the soil had a high capacity for net nitrification, and the vegetation was totally dominated by potentially AM or nonmycorrhizal herbs, some of which had high foliar nitrate reductase activity. Foliar and root N concentrations increased steeply towards the discharge area, but foliar P/N ratios declined below critical levels at the end of the transect. Root 32P uptake bioassays also indicated a P deficiency in the discharge area, where the soil total P content was high, while the concentration of P04 in the soil solution was very low. The high capacity of the mor in the discharge area to adsorb P04, due to the presence of organically complexed Fe and Fe-oxihydroxides, may explain the low P04 concentrations. Our data indicate that the underlying factors influencing both productivity and com- munity composition are pH and supply of base cations. Fundamental differences in exchange characteristics of soil and soil water underlie other related nutrient supply features, in particular the amount and availability of N. Our study of a single short topographic transect supported a previous suggestion based on a regional survey in Norway that variability in soil pH and the supply of base cations affects plant productivity and community composition via effects on N supply. Our data also encompass the interrelations between soil pH, soil N turnover, and the mycorrhizal type of dominant plant species, which, according to Read (1991), occur along long latitudinal or altitudinal climatic gradients. Through millennia discharge areas like the one observed by us have probably provided a relatively stable environment for plants demanding high soil pH and N supply, at the same time as sur- rounding recharge areas have been acidified naturally through podzolization.

Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics.

In this review, we synthesize field and culture studies of the 15N/14N (expressed as δ15N) of autotrophic plants, mycoheterotrophic plants, parasitic plants, soil, and mycorrhizal fungi to assess the major controls of isotopic patterns. One major control for plants and fungi is the partitioning of nitrogen (N) into either 15N-depleted chitin, ammonia, or transfer compounds or 15N-enriched proteinaceous N. For example, parasitic plants and autotrophic hosts are similar in δ15N (with no partitioning between chitin and protein), mycoheterotrophic plants are higher in δ15 N than their fungal hosts, presumably with preferential assimilation of fungal protein, and autotrophic, mycorrhizal plants are lower in 15N than their fungal symbionts, with saprotrophic fungi intermediate, because mycorrhizal fungi transfer 15N-depleted ammonia or amino acids to plants. Similarly, nodules of N2-fixing bacteria transferring ammonia are often higher in δ15N than their plant hosts. N losses via denitrification greatly influence bulk soil δ15N, whereas δ15N patterns within soil profiles are influenced both by vertical patterns of N losses and by N transfers within the soil-plant system. Climate correlates poorly with soil δ15N; climate may primarily influence δ15N patterns in soils and plants by determining the primary loss mechanisms and which types of mycorrhizal fungi and associated vegetation dominate across climatic gradients.

Fertile forests produce biomass more efficiently

Trees with sufficient nutrition are known to allocate carbon preferentially to aboveground plant parts. Our global study of 49 forests revealed an even more fundamental carbon allocation response to nutrient availability: forests with high-nutrient availability use 58 ± 3% (mean ± SE; 17 forests) of their photosynthates for plant biomass production (BP), while forests with low-nutrient availability only convert 42 ± 2% (mean ± SE; 19 forests) of annual photosynthates to biomass. This nutrient effect largely overshadows previously observed differences in carbon allocation patterns among climate zones, forest types and age classes. If forests with low-nutrient availability use 16 ± 4% less of their photosynthates for plant growth, what are these used for? Current knowledge suggests that lower BP per unit photosynthesis in forests with low- versus forests with high-nutrient availability reflects not merely an increase in plant respiration, but likely results from reduced carbon allocation to unaccounted components of net primary production, particularly root symbionts.