•A low N supply limits plant production in most boreal forests, but N-rich spots occur.•The rate of decomposition does not limit the rate of N supply in N-limited forests.•There, tree C allocation to ...mycorrhizal fungi exerts a pivotal control on N cycling.•In N-limited forests mycorrhizal fungi retain much N and transfer little to trees.•The mycorrhizal N sink is weakened by clear-felling, which promotes seedling growth.
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.
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.
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 13CO2 absorbed through tree photosynthesis and 15N injected into a soil layer in which ectomycorrhizal fungi dominate the microbial community.
We detected little 15N 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 15N 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.
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 ¹³C 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 in the late (August) season compared with the early season (June). Labelled 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 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.
In Fennoscandian boreal forests, soil pH and N supply generally increase downhill as a result of water transport of base cations and N, respectively. Simultaneously, forest productivity increases, ...the understory changes from ericaceous dwarf shrubs to tall herbs; in the soil, fungi decrease whereas bacteria increase. The composition of the soil microbial community is mainly thought to be controlled by the pH and C-to-N ratio of the substrate. However, the latter also determines the N supply to plants, the plant community composition, and should also affect plant allocation of C below ground to roots and a major functional group of microbes, mycorrhizal fungi. We used phospholipid fatty acids (PLFAs) to analyze the potential importance of mycorrhizal fungi by comparing the microbial community composition in a tree-girdling experiment, where tree belowground C allocation was terminated, and in a long-term (34 years) N loading experiment, with the shifts across a natural pH and N supply gradient. Both tree girdling and N loading caused a decline of ca. 45% of the fungal biomarker PLFA 18:2ω6,9, suggesting a common mechanism, i.e., that N loading caused a decrease in the C supply to ectomycorrhizal fungi just as tree girdling did. The total abundance of bacterial PLFAs did not respond to tree girdling or to N loading, in which cases the pH (of the mor layer) did not change appreciably, but bacterial PLFAs increased considerably when pH increased across the natural gradient. Fungal biomass was high only in acid soil (pH < 4.1) with a high C-to-N ratio (>38). According to a principal component analysis, the soil C-to-N ratio was as good as predictor of microbial community structure as pH. Our study thus indicated the soil C-to-N ratio, and the response of trees to this ratio, as important factors that together with soil pH influence soil microbial community composition.
•Mycorrhizal mycelia can connect trees and seedlings.•Carbon and nutrients can be transported through the mycelium.•Trees may potentially nourish their offspring via mycelial ...interconnections.•Severing of mycelial connections improves seedling growth in boreal forests.•Conflicting evidence calls for more experimental work in the field.
Forest soil organic matter (SOM) is an important dynamic store of C and N, which releases plant available N and the greenhouse gases CO2 and N2O. Early stages of decomposition of recent plant litters ...are better known than the formation of older and more stable soil pools of N and C, in which case classic theory stated that selective preservation of more resistant plant compounds was important. Recent insights heighten that all plant matter becomes degraded and that older SOM consists of compounds proximally of microbial origin. It has been proposed that in boreal forests, ectomycorrhizal fungi (ECMF), symbionts of trees, are actively involved in the formation of slowly-degrading SOM.
We characterized SOM in the mor-layer along a local soil N supply gradient in a boreal forest, a gradient with large variations in chemical and biological characteristics, notably a decline in the biomass of ECMF in response to increasing soil N supply.
We found contrasting and regular patterns in carbohydrates, lignin, aromatic carbon, and in N-containing compounds estimated by solid-state 13C and 15N nuclear magnetic resonance (NMR) spectroscopy. These occurred along with parallel changes in the natural abundances of the stable isotopes 13C and 15N in both bulk SOM and extracted fractions of the SOM. The modelled “bomb-14C″ age of the lower layers studied ranged between 15 years at the N-poor end, to 70 years at the N-rich end of the gradient. On average half the increase in δ13C with soil depth (and hence age) of the mor-layer can be attributed to soil processes and the other half to changes in the isotopic composition of the plant C inputs. There was a decrease in carbohydrates (O-alkyl C) with increasing depth. This supports the classical hypothesis of declining availability of easily decomposable substrates to microorganisms with increasing soil depth and age. The observed increase in δ13C with depth, however, speaks against the idea of selective preservation of more resistant plant compounds like lignin. Furthermore, from the N-poor to the N-rich end the difference between 15N in plant litter N and N in the deeper part of the mor-layer, the H-layer, decreased in parallel with a decline in ECMF.
The latter provides evidence that the role of ECMF as major sink for N diminishes, and hence their potential role in SOM stabilization, when the soil N supply increases. At the N-rich end, where bacteria dominate over fungi, other agents than ECMF must be involved in the large build-up of the H-layer with the slowest turnover rate found along the gradient.
•Ectomycorrhizal fungi (ECMF) have been proposed as key agents of SOM formation.•We show that this may occur in N-poor boreal soils.•The largest buildup of SOM occurred at low abundance of ECMF in N-rich soils.
Summary
Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or ‘mother trees’, support ...the growth of seedlings in this way. This narrative has far‐reaching implications for our understanding of forest ecology and has been controversial in the scientific community. We review the current understanding of ectomycorrhizal C metabolism and observations on forest regeneration that make the mother tree narrative debatable. We then re‐examine data and conclusions from publications that underlie the mother tree hypothesis. Isotopic labeling methods are uniquely suited for studying element fluxes through ecosystems, but the complexity of mycorrhizal symbiosis, low detection limits, and small carbon discrimination in biological processes can cause researchers to make important inferences based on miniscule shifts in isotopic abundance, which can be misleading. We conclude that evidence of a significant net C transfer via common mycorrhizal networks that benefits the recipients is still lacking. Furthermore, a role for fungi as a C pipeline between trees is difficult to reconcile with any adaptive advantages for the fungi. Finally, the hypothesis is neither supported by boreal forest regeneration patterns nor consistent with the understanding of physiological mechanisms controlling mycorrhizal symbiosis.
•We studied the soil C/N ratio, a metric of plant N supply, from N. Sweden to Germany.•The plant N supply increases substantially from N. Sweden to Germany in the south.•Forest management operations ...can cause losses of N from N–rich soils.•Where soils are N–poor, management needs to enhance the N supply to tree seedlings.•The results speak against the use of a single management method in Sweden and Germany.
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 in c. 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.
• Trees reduce their carbon (C) allocation to roots and mycorrhizal fungi in response to high nitrogen (N) additions, which should reduce the N retention capacity of forests. The time needed for ...recovery of mycorrhizas after termination of N loading remains unknown. • Here, we report the long‐term impact of N loading and the recovery of ectomycorrhiza after high N loading on a Pinus sylvestris forest. We analysed the N% and abundance of the stable isotope ¹⁵N in tree needles and soil, soil microbial fatty acid biomarkers and fungal DNA. • Needles in N‐loaded plots became enriched in ¹⁵N, reflecting decreased N retention by mycorrhizal fungi and isotopic discrimination against ¹⁵N during loss of N. Meanwhile, needles in N‐limited (control) plots became depleted in ¹⁵N, reflecting high retention of ¹⁵N by mycorrhizal fungi. N loading was terminated after 20 yr. The δ¹⁵N and N% of the needles decreased 6 yr after N loading had been terminated, and approached values in control plots after 15 yr. This decrease, and the larger contributions compared with N‐loaded plots of a fungal fatty acid biomarker and ectomycorrhizal sequences, suggest recovery of ectomycorrhiza. • High N loading rapidly decreased the functional role of ectomycorrhiza in the forest N cycle, but significant recovery occurred within 6-15 yr after termination of N loading.
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