What happens to trees and soils during five decades of experimental nitrogen loading?

High deposition of nitrogen was postulated to drive losses of NO3 - and nutrient base cations, causing soil acidification, nutrient deficiencies reducing tree growth and ultimately tree mortality. We tested these predictions in a uniquely long-term study involving three NH4NO3 addition treatments (N1-N3) in a boreal Pinus sylvestris forest. The lowest level (N1), 30 kg N ha− 1 yr− 1 was applied during 50 years. Twice this rate (N2) was added 38 years, followed by 12 years of recovery, while thrice this rate (N3) was added 20 years followed by 30 years of recovery. We compared tree growth, changes in foliar and soil chemistry among treatments including control plots without N additions. As predicted, the N treatments lowered soil pH and reduced soil base saturation by around 50 %. They also lowered foliar levels of Ca, Mg, K, P and B initially, but after 50 years only Ca and Mg remained lower than in the control. Lack of B motivated a single addition of 2.5 kg ha− 1 after ten years of N treatment. Tree stem growth became and then remained higher in N1 than in the other treatments through the 50 years of treatments. In N2 and N3, foliar δ15N increased during the N-loading phase, but declined during the recovery phase, indicating a return of ectomycorrhizal fungi and their role in tightening the N cycle in N-limited forests. In the terminated, initially highest N treatments, N2 and N3, the trees even show signs of returning to Nlimitation. In these treatments, the soil base saturation remains lower, while the pH was only lower at 0–10 depth in the mineral soil, but not in the 10–20 cm depth horizon or in the superficial organic mor-layer. Accurately documenting the effect of N additions on forest growth required a long-term approach, where reasonable rates of application could be compared with extreme rates. Such long-term experiments are necessary to support forest management in achieving goals for developing future forests as they shift in response to major, global-scale changes

Shifts in soil microbial community structure, nitrogen cycling and the concomitant declining N availability in ageing primary boreal forest ecosystems

AbstractPlant growth in boreal forests is commonly limited by a low supply of nitrogen, a condition that may be aggravated by high tree below-ground allocation of carbon to ectomycorrhizal (ECM) fungi and associated microorganisms. These in turn immobilise N and reduce its availability to plants as boreal ecosystems develop. Here, we studied a boreal forest ecosystem chronosequence created by new land rising out of the sea due to iso-static rebound along the coast of northern Sweden. We used height over the ocean to estimate ecosystem age and examined its relationship to soil microbial community structure and the gross turnover of N. The youngest soils develop with meadows by the coast, followed by a zone of N2-fixing alder trees, and primary boreal conifer forest on ground up to 560 years old. The young soils in meadows contained little organic matter and microbial biomass per unit area. Nitrogen was turned over at low rates when expressed per area (m−2), but specific rates (per gram soil carbon (C)) were the highest found along the transect. In the zone with alder, the amounts of soil C and microbial biomass were much higher (bacterial biomass had doubled and fungal biomass quadrupled). Rates of gross N mineralisation (expressed on an area basis) were highest, but the retention of added labelled NH4+ was lowest in this soil as compared to other ages. The alder zone also had the largest extractable pools of inorganic N in soil and highest N % in plant foliage. In the older conifer forest ecosystems the amounts of soil C and N, as well as biomass of both bacteria and fungi increased. Data on organic matter 14C suggested that the largest input of recently fixed plant C occurred in the younger coniferous forest ecosystems. With increasing ecosystem age, the ratio of microbial C to total soil C was constant, whereas the ratio of microbial N to total soil N increased and gross N mineralization declined. Simultaneously, plant foliar N % decreased and the natural abundance of 15N in the soil increased. More specifically, the difference in δ15N between plant foliage and soil increased, which is related to relatively greater retention of 15N relative to 14N by ECM fungi as N is taken up from the soil and some N is transferred to the plant host. In the conifer forest, where these changes were greatest, we found increased fungal biomass in the F- and H-horizons of the mor-layer, in which ECM fungi are known to dominate (the uppermost horizon with litter and moss is dominated by saprotrophic fungi). Hence, we propose that the decreasing availability of N to the plants and the subsequent decline in plant production in ageing boreal forests is linked to high tree belowground C allocation to ECM fungi, a strong microbial sink for available soil N

Tamm Review: On the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests

The supply of nitrogen commonly limits plant production in boreal forests and also affects species composition and ecosystem functions other than plant growth. These interrelations vary across the landscapes, with the highest N availability, plant growth and plant species richness in ground-water discharge areas (GDAs), typically in toe-slope positions, which receive solutes leaching from the much larger groundwater recharge areas (GRAs) uphill. Plant N sources include not only inorganic N, but, as heightened more recently, also organic N species. In general, also the ratio inorganic N over organic N sources increase down hillslopes. Here, we review recent evidence about the nature of the N limitation and its variations in Fennoscandian boreal forests and discuss its implications for forest ecology and management. The rate of litter decomposition has traditionally been seen as the determinant of the rate of N supply. However, while N-rich litter decomposes faster than N-poor litter initially, N-rich litter then decomposes more slowly, which means that the relation between N % of litter and its decomposability is complex. Moreover, in the lower part of the mor-layer, where the most superficial mycorrhizal roots first appear, and N availability matters for plants, the ratio of microbial N over total soil N is remarkably constant over the wide range in litter and soil C/N ratios of between 15 and 40 for N-rich and N-poor sites, respectively. Nitrogen-rich and -poor sites thus differ in the sizes of the total N pool and the microbial N pool, but not in the ratio between them. A more important difference is that the soil microbial N pool turns over faster in N-rich systems because the microbes are more limited by C, while microbes in N-poor systems are a stronger sink for available N. Furthermore, litter decomposition in the most superficial soil horizon (as studied by the so-called litter-bag method) is associated with a dominance of saprotrophic fungi, and absence of mycorrhizal fungi. The focal zone in the context of plant N supply in N-limited forests is further down the soil profile, where ectomycorrhizal (ECM) roots become abundant. Molecular evidence and stable isotope data indicate that in the typical N-poor boreal forests, nitrogen is retained in saprotrophic fungi, likely until they run out of energy (available C-compounds). Then, as heightened by recent research, ECM fungi, which are supplied by photosynthate from the trees, become the superior competitors for N. In N-poor boreal soils strong N retention by microorganisms keeps levels of available N very low. This is exacerbated by an increase in tree C allocation to mycorrhizal fungi (TCAM) relative to net primary production (NPP) with decreasing soil N supply, which causes ECM fungi to retain much of the available soil N for their own growth and transfer little to their tree hosts. The transfer of N through the ECM fungi, and not the rate of litter decomposition, is likely limiting the rate of tree N supply under such conditions. All but a few stress-tolerant less N-demanding plant species, like the ECM trees themselves and ericaceous dwarf shrubs, are excluded. With increasing N supply, a weakening of ECM symbiosis caused by the relative decline in TCAM contributes to shifts in soil microbial community composition from fungal dominance to bacterial dominance. Thus, bacteria, which are less C-demanding, but more likely to release N than fungi, take over. This, and the relatively high pH in GDA, allow autotrophic nitrifying bacteria to compete successfully for the NH4+ released by C-limited organisms and causes the N cycle to open up with leaching of nitrate (NO3−) and gaseous N losses through denitrification. These N-rich conditions allow species-rich communities of N-demanding plant species. Meanwhile, ECM fungi have a smaller biomass, are supplied with N in excess of their demand and will export more N to their host trees. Hence, the gradient from low to high N supply is characterized by profound variations in plant and soil microbial physiologies, especially their relations to the C-to-N supply ratio. We propose how interactions among functional groups can be understood and modelled (the plant-microbe carbon-nitrogen model). With regard to forest management these perspectives explain why the creation of larger tree-free gaps favors the regeneration of tree seedlings under N-limited conditions through reduced belowground competition for N, and why such gaps are less important under high N supply (but when light might be limiting). We also discuss perspectives on the relations between N supply, biodiversity, and eutrophication of boreal forests from N deposition or forest fertilization

Carbon-nitrogen relations of ectomycorrhizal mycelium across a natural nitrogen supply gradient in boreal forest

The supply of carbon (C) from tree photosynthesis to ectomycorrhizal (ECM) fungi is known to decrease with increasing plant nitrogen (N) supply, but how this affects fungal nutrition and growth remains to be clarified. We placed mesh-bags with quartz sand, with or without an organic N (N-15-, C-13-labeled) source, in the soil along a natural N supply gradient in boreal forest, to measure growth and use of N and C by ECM extramatrical mycelia. Mycelial C : N declined with increasing N supply. Addition of N increased mycelial growth at the low-N end of the gradient. We found an inverse relationship between uptake of added N and C; the use of added N was high when ambient N was low, whereas use of added C was high when C from photosynthesis was low. We propose that growth of ECM fungi is N-limited when soil N is scarce and tree belowground C allocation to ECM fungi is high, but is C-limited when N supply is high and tree belowground C allocation is low. This suggests that ECM fungi have a major role in soil N retention in nutrient-poor, but less so in nutrient-rich boreal forests

Large differences in plant nitrogen supply in German and Swedish forests - Implications for management

In European forests, plant N supply varies from regions where N deposition is negligible and a low natural N supply limits production to regions where high N deposition adds to a high natural N supply. Here, we ask if the differences in N supply are too large to make one system of management for wood production, continuous-cover forestry or rotational forestry, optimal across these conditions.We analyzed the C/N ratio inc. 8400 samples of surficial soil layers along a 2400 km long transect through Sweden and Germany to obtain a quantitative description of differences in plant N supply. We discuss the differences in relation to forest management, especially evidence that soil C/N ratios below 25 are associated with higher N supply, risks of leaching of nitrate, and gaseous losses of N2O, whereas ratios above 25 are associated with a tighter N cycle and an N limitation to tree growth.The percent soil with C/N ratios above 25 declines from 91 in N. Norrland in Sweden to 26 in Germany. Simultaneously, mor soils (with a distinct organic layer on top of the mineral soil) decline from 95% to 16%, while mull soils (in which organic matter and mineral particles are mixed) increase from 1% to 40%. However, low C/N ratios also occur in the north, where we find the largest width in C/N ratios from 16 in mull soils to 36 in mor soils, which compares with a variation in Germany from 17 to 27. Soils under conifers generally have higher C/N ratios than soils under broadleaves, but our survey data cannot support that the trees are the sole cause of this pattern. Very low C/N ratios occur in conifer-dominated forests in the north.The high incidence (74%) of C/N ratios below 25 indicates that forest management in Germany should use methods, which minimize the risk of N losses. Continuous-cover forestry may fulfill that objective. In the north with 9% of the soils below this threshold, risks of N losses are small. There, rotational forestry involving clear-felling alleviates the competition for soil N from larger trees allowing successful regeneration of tree seedlings. From the perspective of interactions between plant N supply and management of forests for wood production, no single management system seems optimal along this large gradient. We propose that research on forest management systems should address the importance of N supply

Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis

Ectomycorrhizal symbiosis is omnipresent in boreal forests, where it is assumed to benefit plant growth. However, experiments show inconsistent benefits for plants and volatility of individual partnerships, which calls for a re-evaluation of the presumed role of this symbiosis. We reconcile these inconsistencies by developing a model that demonstrates how mycorrhizal networking and market mechanisms shape the strategies of individual plants and fungi to promote symbiotic stability at the ecosystem level. The model predicts that plants switch abruptly from a mixed strategy with both mycorrhizal and nonmycorrhizal roots to a purely mycorrhizal strategy as soil nitrogen availability declines, in agreement with the frequency distribution of ectomycorrhizal colonization intensity across a wide-ranging data set. In line with observations in field-scale isotope labeling experiments, the model explains why ectomycorrhizal symbiosis does not alleviate plant nitrogen limitation. Instead, market mechanisms may generate self-stabilization of the mycorrhizal strategy via nitrogen depletion feedback, even if plant growth is ultimately reduced. We suggest that this feedback mechanism maintains the strong nitrogen limitation ubiquitous in boreal forests. The mechanism may also have the capacity to eliminate or even reverse the expected positive effect of rising CO2 on tree growth in strongly nitrogen-limited boreal forests