Natural Abundance of <Superscript>15</Superscript>N in Nitrogen-Limited Forests and Tundra Can Estimate Nitrogen Cycling Through Mycorrhizal Fungi: A Review

The hyphae of ectomycorrhizal and ericoid mycorrhizal fungi proliferate in nitrogen (N)-limited forests and tundra where the availability of inorganic N is low; under these conditions the most common fungal species are those capable of protein degradation that can supply their host plants with organic N. Although it is widely understood that these symbiotic fungi supply N to their host plants, the transfer is difficult to quantify in the field. A novel approach uses the natural ¹⁵N:¹⁴N ratios (expressed as δ¹⁵N values) in plants, soils, and mycorrhizal fungi to estimate the fraction of N in symbiotic trees and shrubs that enters through mycorrhizal fungi. This calculation is possible because mycorrhizal fungi discriminate against ¹⁵N when they create compounds for transfer to plants; host plants are depleted in ¹⁵N, whereas mycorrhizal fungi are enriched in ¹⁵N. The amount of carbon (C) supplied to these fungi can be stoichiometrically calculated from the fraction of plant N derived from the symbiosis, the N demand of the plants, the fungal C:N ratio, and the fraction of N retained in the fungi. Up to a third of C allocated belowground, or 20% of net primary production, is used to support ectomycorrhizal fungi. As anthropogenic N inputs increase, the C allocation to fungi decreases and plant δ¹⁵N increases. Careful analyses of δ¹⁵N patterns in systems dominated by ectomycorrhizal and ericoid mycorrhizal symbioses may reveal the ecosystem-scale effects of alterations in the plant–mycorrhizal symbioses caused by shifts in climate and N deposition. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Site-dependent N uptake from N-form mixtures by arctic plants,soil microbes and ectomycorrhizal fungi

Soil microbes constitute an important control on nitrogen (N) turnover and retention in arctic ecosystems where N availability is the main constraint on primary production. Ectomycorrhizal (ECM) symbioses may facilitate plant competition for the specific N pools available in various arctic ecosystems. We report here our study on the N uptake patterns of coexisting plants and microbes at two tundra sites with contrasting dominance of the circumpolar ECM shrub Betula nana. We added equimolar mixtures of glycine-N, NH₄⁺–N and NO₃⁻–N, with one N form labelled with ¹⁵N at a time, and in the case of glycine, also labelled with ¹³C, either directly to the soil or to ECM fungal ingrowth bags. After 2 days, the vegetation contained 5.6, 7.7 and 9.1% (heath tundra) and 7.1, 14.3 and 12.5% (shrub tundra) of the glycine-, NH₄⁺- and NO₃⁻–¹⁵N, respectively, recovered in the plant–soil system, and the major part of ¹⁵N in the soil was immobilized by microbes (chloroform fumigation-extraction). In the subsequent 24 days, microbial N turnover transferred about half of the immobilized ¹⁵N to the non-extractable soil organic N pool, demonstrating that soil microbes played a major role in N turnover and retention in both tundra types. The ECM mycelial communities at the two tundras differed in N-form preferences, with a higher contribution of glycine to total N uptake at the heath tundra; however, the ECM mycelial communities at both sites strongly discriminated against NO₃⁻. Betula nana did not directly reflect ECM mycelial N uptake, and we conclude that N uptake by ECM plants is modulated by the N uptake patterns of both fungal and plant components of the symbiosis and by competitive interactions in the soil. Our field study furthermore showed that intact free amino acids are potentially important N sources for arctic ECM fungi and plants as well as for soil microorganisms. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions

Nitrogen isotope measurements may provide insights into changing interactions among plants, mycorrhizal fungi, and soil processes across environmental gradients. Here, we report changes in δ¹⁵N signatures due to shifts in species composition and nitrogen (N) dynamics. These changes were assessed by measuring fine root biomass, net N mineralization, and N concentrations and δ¹⁵N of foliage, fine roots, soil, and mineral N across six sites representing different post-deglaciation ages at Glacier Bay, Alaska. Foliar δ¹⁵N varied widely, between 0 and –2‰ for nitrogen-fixing species, between 0 and –7‰ for deciduous non-fixing species, and between 0 and –11‰ for coniferous species. Relatively constant δ¹⁵N values for ammonium and generally low levels of soil nitrate suggested that differences in ammonium or nitrate use were not important influences on plant δ¹⁵N differences among species at individual sites. In fact, the largest variation among plant δ¹⁵N values were observed at the youngest and oldest sites, where soil nitrate concentrations were low. Low mineral N concentrations and low N mineralization at these sites indicated low N availability. The most plausible mechanism to explain low δ¹⁵N values in plant foliage was a large isotopic fractionation during transfer of nitrogen from mycorrhizal fungi to plants. Except for N-fixing plants, the foliar δ¹⁵N signatures of individual species were generally lower at sites of low N availability, suggesting either an increased fraction of N obtained from mycorrhizal uptake (f), or a reduced proportion of mycorrhizal N transferred to vegetation (T _r). Foliar and fine root nitrogen concentrations were also lower at these sites. Foliar N concentrations were significantly correlated with δ¹⁵N in foliage of Populus, Salix, Picea, and Tsuga heterophylla, and also in fine roots. The correlation between δ¹⁵N and N concentration may reflect strong underlying relationships among N availability, the relative allocation of carbon to mycorrhizal fungi, and shifts in either f or T _r. Received: 14 December 1998 / Accepted: 16 August 1999     

Linkages between N turnover and plant community structure in a tundra landscape

The spatial distribution of organic soil nitrogen (N) in alpine tundra was studied along a natural environmental gradient, covering five plant communities, at the Latnjajaure Field Station, northern Swedish Lapland. The five communities (mesic meadow, meadow snowbed, dry heath, mesic heath, and heath snowbed) are the dominant types in this region and are differentiated by soil pH. Net N mineralization, net ammonification, and net nitrification were measured using 40-day laboratory incubations based on extractable NH₄⁺ and NO₃⁻. Nitrification enzyme activity (NEA), denitrification enzyme activity (DEA), amino acid concentrations, and microbial respiration were measured for soils from each plant community. The results show that net N mineralization rates were more than three times higher in the meadow ecosystems (mesic meadow 0.7 μg N g⁻¹ OM day⁻¹ and meadow snowbed 0.6 μg N g⁻¹ OM day⁻¹) than the heath ecosystems (dry heath 0.2 μg N g⁻¹ OM day⁻¹, mesic heath 0.1 μg N g⁻¹ OM day⁻¹ and heath snowbed 0.2 μg N g⁻¹ OM day⁻¹). The net N mineralization rates were negatively correlated to organic soil C/N ratio (r = −0.652, P < 0.001) and positively correlated to soil pH (r = 0.701, P < 0.001). Net nitrification, inorganic N concentrations, and NEA rates also differed between plant communities; the values for the mesic meadow were at least four times higher than the other plant communities, and the snowbeds formed an intermediate group. Moreover, the results show a different pattern of distribution for individual amino acids across the plant communities, with snowbeds tending to have the highest amino acid N concentrations. The differences between plant communities along this natural gradient also illustrate variations between the dominant mycorrhizal associations in facilitating N capture by the characteristic functional groups of plants. Responsible Editor: Bernard Nicolardot     

Plant and soil natural abundance <Emphasis Type="Italic">δ</Emphasis><Superscript>15</Superscript>N: indicators of relative rates of nitrogen cycling in temperate forest ecosystems

Watersheds within the Catskill Mountains, New York, receive among the highest rates of nitrogen (N) deposition in the northeastern United States and are beginning to show signs of N saturation. Despite similar amounts of N deposition across watersheds within the Catskill Mountains, rates of soil N cycling and N retention vary significantly among stands of different tree species. We examined the potential use of δ ¹⁵N of plants and soils as an indicator of relative forest soil N cycling rates. We analyzed the δ ¹⁵N of foliage, litterfall, bole wood, surface litter layer, fine roots and organic soil from single-species stands of American beech (Fagus grandifolia), eastern hemlock (Tsuga canadensis), red oak (Quercus rubra), and sugar maple (Acer saccharum). Fine root and organic soil δ ¹⁵N values were highest within sugar maple stands, which correlated significantly with higher rates of net mineralization and nitrification. Results from this study suggest that fine root and organic soil δ ¹⁵N can be used as an indicator of relative rates of soil N cycling. Although not statistically significant, δ ¹⁵N was highest within foliage, wood and litterfall of beech stands, a tree species associated with intermediate levels of soil N cycling rates and forest N retention. Our results show that belowground δ ¹⁵N values are a better indicator of relative rates of soil N cycling than are aboveground δ ¹⁵N values.     

Biogeochemical pools and fluxes of carbon and nitrogen in a maritime tundra near penguin colonies along the Antarctic Peninsula

There is limited information regarding biogeochemical pools and fluxes in maritime tundra ecosystems along the Antarctic Peninsula. To collect baseline information on biogeochemical processes in a tundra ecosystem dominated by two vascular plant species (Colobanthus quitensis and Deschampsia antarctica) at Biscoe Point off the coast of Anvers Island, we measured pools and fluxes of C and N in transplanted tundra microcosm cores, complemented with sampling of precipitation and surface runoff. Snow and snowmelt from the tundra collection site and soil leachates from the cores were enriched with N and dissolved organic carbon compared to precipitation and snowmelt samples collected at Palmer Station, indicating high loading of N and organic matter from the penguin colonies adjacent to the tundra site. Relatively high values of δ¹⁵N in the live and dead biomass of D. antarctica and C. quitensis (5.6–25.1‰) indicated an enrichment of N in this tundra ecosystem, possibly through N inputs from adjacent penguin colonies. Stepwise multiple linear regressions found that ecosystem respiration and gross primary production were best predicted by live biomass of D. antarctica, suggesting a disproportionately high contribution of D. antarctica to CO₂ fluxes. The cores with higher δ¹⁵N and lower δ¹³C in the soil organic horizon exhibited higher CO₂ fluxes. The results suggest that abundant N inputs from penguin colonies and the competitive balance between plant species might play a critical role in the response of tundra ecosystems along the Antarctic Peninsula to projected climate change.     

Contrasts Among Mycorrhizal Plant Guilds in Foliar Nitrogen Concentration and δ15N Along Productivity Gradients of a Boreal Forest

The distribution of plant species in boreal forest understories is hypothesized to reflect mycorrhizal guilds and associated adaptations for organic nitrogen (N) acquisition. In this study of a natural edaphic gradient, where supply rates of inorganic N increase with site productivity, we noted a decline in understory ectomycorrhizal, ericoid, and arbutoid plant communities on productive sites, in contrast to a positive response by most arbuscular species. We then assessed the rate of change in foliar N concentration (N_conc) and abundance of ¹⁵N (δ¹⁵N) of select plants from these mycorrhizal guilds. Two arbuscular plant species (Rubus parviflorus and Viburnum edule) had the sharpest increases in foliar N_conc with enhanced supplies of NH₄ ⁺ and NO₃ ⁻, but with no differences in foliar δ¹⁵N. An ectomycorrhizal species, Abies lasiocarpa, and ericoid species, Vaccinium membranaceum, had parallel increases in both N_conc and δ¹⁵N with soil N supply. The foliar δ¹⁵N of two arbutoid plants (Orthilia secunda and Pyrola asarifolia) were as enriched as ectomycorrhizal sporocarps, likely indicating N transfer from mycorrhizal networks. The depletion of foliar δ¹⁵N by ectomycorrhizal and ericoid plants on poorer sites likely reflected a high degree of N retention and photosynthate demand by fungi, whereas arbuscular plants may have had a less significant δ¹⁵N response because of a more passive role by fungi in scavenging organic N. The results suggest differences in how mycorrhiza exploit diverse soil N supplies (recalcitrant and labile organic N, NH₄ ⁺, NO₃ ⁻, and parasitized N) could be an important factor in boreal plant community composition.     

Leaf 15N abundance of subarctic plants provides field evidence that ericoid,ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen

The natural abundance of the nitrogen isotope 15, ¹⁵N, was analysed in leaves of 23 subarctic vascular plant species and two lichens from a tree-line heath at 450 m altitude and a fellfield at 1150 m altitude close to Abisko in N. Sweden, as well as in soil, rain and snow. The aim was to reveal if plant species with different types of mycorrhizal fungi also differ in their use of the various soil N sources. The dwarf shrubs and the shrubs, which in combination formed more than 65% of the total above-ground biomass at both sites, were colonized by ericoid or ectomycorrhizal fungi. Their leaf ¹⁵N was between–8.8 and–5.5 at the heath and between–6.1 and –3.3 at the fellfield. The leaf ¹⁵N of non- or arbuscular mycorrhizal species was markedly different, ranging from –4.1 to –0.4 at the heath, and from –3.4 to+2.2 at the fellfield. We conclude that ericoid and ectomycorrhizal dwarf shrubs and shrubs utilize a distinct N source, most likely a fraction of the organic N in fresh litter, and not complexed N in recalcitrant organic matter. The latter is the largest component of soil total N, which had a ¹⁵N of –0.7 at the heath and +0.5 at the fellfield. Our field-based data thus support earlier controlled-environment studies and studies on the N uptake of excised roots, which have demonstrated protease activity and amino acid uptake by ericoid and ectomycorrhizal tundra species. The leaves of ectomycorrhizal plants had slightly higher ¹⁵N (fellfield) and N concentration than leaves of the ericoids, and Betula nana, Dryas octopetala and Salix spp. also showed NO _inf3 ^sup- reductase activity. These species may depend more on soil inorganic N than the ericoids. The ¹⁵N of non- or arbuscular mycorrhizal species indicates that the ¹⁵N of inorganic N available to these plants was higher than that of average fresh litter, probably due to high microbial immobilization of inorganic N. The ¹⁵N of NH _inf4 ^sup+ -N was +12.3 in winter snow and +1.9 in summer rain. Precipitation N might be a major contributer in species with poorly developed root systems, e.g. Lycopodium selago. Our results show that coexisting plant species under severe nutrient limitation may tap several different N sources: NH _inf4 ^sup+ , NO _inf3 ^sup- and organic N from the soil, atmospheric N₂, and N in precipitation. Ericoid and ectomycorrhizal fungi are of major importance for plant N uptake in tundra ecosystems, and mycorrhizal fungi probably exert a major control on plant ¹⁵N in organic soils.     

Foliar and fungal <Superscript>15</Superscript> N:<Superscript>14</Superscript> N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models

Nitrogen isotopes (¹⁵N/¹⁴N ratios, expressed as δ¹⁵N values) are useful markers of the mycorrhizal role in plant nitrogen supply because discrimination against ¹⁵N during creation of transfer compounds within mycorrhizal fungi decreases the ¹⁵N/¹⁴N in plants (low δ¹⁵N) and increases the ¹⁵N/¹⁴N of the fungi (high δ¹⁵N). Analytical models of ¹⁵N distribution would be helpful in interpreting δ¹⁵N patterns in fungi and plants. To compare different analytical models, we measured nitrogen isotope patterns in soils, saprotrophic fungi, ectomycorrhizal fungi, and plants with different mycorrhizal habits on a glacier foreland exposed during the last 100 years of glacial retreat and on adjacent non-glaciated terrain. Since plants during early primary succession may have only limited access to propagules of mycorrhizal fungi, we hypothesized that mycorrhizal plants would initially be similar to nonmycorrhizal plants in δ¹⁵N and then decrease, if mycorrhizal colonization were an important factor influencing plant δ¹⁵N. As hypothesized, plants with different mycorrhizal habits initially showed similar δ¹⁵N values (−4 to −6‰ relative to the standard of atmospheric N₂ at 0‰), corresponding to low mycorrhizal colonization in all plant species and an absence of ectomycorrhizal sporocarps. In later successional stages where ectomycorrhizal sporocarps were present, most ectomycorrhizal and ericoid mycorrhizal plants declined by 5–6‰ in δ¹⁵N, suggesting transfer of ¹⁵N-depleted N from fungi to plants. The values recorded (−8 to −11‰) are among the lowest yet observed in vascular plants. In contrast, the δ¹⁵N of nonmycorrhizal plants and arbuscular mycorrhizal plants declined only slightly or not at all. On the forefront, most ectomycorrhizal and saprotrophic fungi were similar in δ¹⁵N (−1 to −3‰), but the host-specific ectomycorrhizal fungus Cortinarius tenebricus had values of up to 7‰. Plants, fungi and soil were at least 4‰ higher in δ¹⁵N from the mature site than in recently exposed sites. On both the forefront and the mature site, host-specific ectomycorrhizal fungi had higher δ¹⁵N values than ectomycorrhizal fungi with a broad host range. From these isotopic patterns, we conclude:(1) large enrichments in ¹⁵N of many ectomycorrhizal fungi relative to co-occurring ectomycorrhizal plants are best explained by treating the plant-fungal-soil system as a closed system with a discrimination against ¹⁵N of 8–10‰ during transfer from fungi to plants, (2) based on models of ¹⁵N mass balance, ericoid and ectomycorrhizal fungi retain up to two-thirds of the N in the plant-mycorrhizal system under the N-limited conditions at forefront sites, (3) sporocarps are probably enriched in ¹⁵N by an additional 3‰ relative to available nitrogen, and (4) host-specific ectomycorrhizal fungi may transfer more N to plant hosts than non-host-specific ectomycorrhizal fungi. Our study confirms that nitrogen isotopes are a powerful tool for probing nitrogen dynamics between mycorrhizal fungi and associated plants.     

Foliar <Superscript>15</Superscript>N natural abundance indicates phosphorus limitation of bog species

Foliar δ¹⁵N, %N and %P in the dominant woody and herbaceous species across nutrient gradients in New Zealand restiad (family Restionaceae) raised bogs revealed marked differences in plant δ¹⁵N correlations with P. The two heath shrubs, Leptospermum scoparium (Myrtaceae) and Dracophyllum scoparium (Epacridaceae), showed considerable isotopic variation (−2.03 to −15.55‰, and −0.39 to −12.06‰, respectively) across the bogs, with foliar δ¹⁵N strongly and positively correlated with P concentrations in foliage and peat, and negatively correlated with foliar N:P ratios. For L. scoparium, the isotopic gradient was not linked to ectomycorrhizal (ECM) fractionation as ECMs occurred only on higher nutrient marginal peats where ¹⁵N depletion was least. In strong contrast, restiad species (Empodisma minus Sporadanthus ferrugineus, S. traversii) showed little isotopic variation across the same nutrient gradients. Empodisma minus and S. traversii had δ¹⁵N levels consistently around 0‰ (means of −0.12‰ and +0.15‰ respectively), and S. ferrugineus, which co-habited with E. minus, was more depleted (mean −4.97‰). The isotopic differences between heath shrubs and restiads were similar in floristically dissimilar bogs and may be linked to contrasting nutrient demands, acquisition mechanisms, and root morphology. Leptospermum scoparium shrubs on low nutrient peats were stunted, with low tissue P concentrations, and high N:P ratios, suggesting they were P-limited, which was probably exacerbated by markedly reduced mycorrhizal colonisations. The coupling of δ¹⁵N depletion and %P in heath shrubs suggests that N fractionation is promoted by P limitation. In contrast, the constancy in δ¹⁵N of the restiad species through the N and P gradients suggests that these are not suffering from P limitation.     

Interpretation of nitrogen isotope signatures using the NIFTE model

Nitrogen cycling in forest soils has been intensively studied for many years because nitrogen is often the limiting nutrient for forest growth. Complex interactions between soil, microbes, and plants and the consequent inability to correlate δ¹⁵N changes with biologic processes have limited the use of natural abundances of nitrogen isotopes to study nitrogen (N) dynamics. During an investigation of N dynamics along the 250-year-old successional sequence in Glacier Bay, Alaska, United States, we observed several puzzling isotopic patterns, including a consistent decline in δ¹⁵N of the late successional dominant Picea at older sites, a lack of agreement between mineral N δ¹⁵N and foliar δ¹⁵N, and high isotopic signatures for mycorrhizal fungi. In order to understand the mechanisms creating these patterns, we developed a model of N dynamics and N isotopes (Nitrogen Isotope Fluxes in Terrestrial Ecosystems, NIFTE), which simulated the major transformations of the N cycle and predicted isotopic signatures of different plant species and soil pools. Comparisons with field data from five sites along the successional sequence indicated that NIFTE can duplicate observed patterns in δ¹⁵N of soil, foliage, and mineral N over time. Different scenarios that could account for the observed isotopic patterns were tested in model simulations. Possible mechanisms included increased isotopic fractionation on mineralization, fractionation during the transfer of nitrogen from mycorrhizal fungi to plants, variable fractionation on uptake by mycorrhizal fungi compared to plants, no fractionation on mycorrhizal transfer, and elimination of mycorrhizal fungi as a pool in the model. The model results suggest that fractionation during mineralization must be small (˜2‰), and that no fractionation occurs during plant or mycorrhizal uptake. A net fractionation during mycorrhizal transfer of nitrogen to vegetation provided the best fit to isotopic data on mineral N, plants, soils, and mycorrhizal fungi. The model and field results indicate that the importance of mycorrhizal fungi to N uptake is probably less under conditions of high N availability. Use of this model should encourage a more rigorous assessment of isotopic signatures in ecosystem studies and provide insights into the biologic transformations which affect those signatures. This should lead to an enhanced understanding of some of the fundamental controls on nitrogen dynamics. Received: 1 July 1998 / Accepted: 23 December 1998     

The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica

This study investigated the nitrogen (N) acquisition from soil and insect capture during the growth of three species of pitcher plants, Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica. ¹⁵N/¹⁴N natural abundance ratios (δ¹⁵N) of plants and pitchers of different age, non-carnivorous reference plants, and insect prey were used to estimate proportional contributions of insects to the N content of leaves and whole plants. Young Nepenthes leaves (phyllodes) carrying closed pitchers comprised major sinks for N and developed mainly from insect N captured elsewhere on the plant. Their δ¹⁵N values of up to 7.2‰ were higher than the average δ¹⁵N value of captured insects (mean δ¹⁵N value = 5.3‰). In leaves carrying old pitchers that are acting as a N source, the δ¹⁵N decreased to 3.0‰ indicating either an increasing contribution of soil N to those plant parts which in fact captured the insects or N gain from N₂ fixation by microorganisms which may exist in old pitchers. The δ¹⁵N value of N in water collected from old pitchers was 1.2‰ and contained free amino acids. The fraction of insect N in young and old pitchers and their associated leaves decreased from 1.0 to 0.3 mg g⁻¹. This fraction decreased further with the size of the investigated tiller. Nepenthes contained on average 61.5 ± 7.6% (mean ± SD, range 50–71%) insect N based on the N content of a whole tiller. In the absence of suitable non-carnivorous reference plants for Cephalotus, δ¹⁵N values were assessed across a developmental sequence from young plants lacking pitchers to large adults with up to 38 pitchers. The data indicated dependence on soil N until 4 pitchers had opened. Beyond that stage, plant size increased with the number of catching pitchers but the fraction of soil N remained high. Large Cephalotus plants were estimated to derive 26 ± 5.9% (mean ± SD of the three largest plants; range: 19–30%) of the N from insects. In Cephalotus we observed an increased δ¹⁵N value in sink versus source pitchers of about 1.2‰ on average. Source and sink pitchers of Darlingtonia had a similar δ¹⁵N value, but plant N in this species showed δ¹⁵N signals closer to that of insect N than in either Cephalotus or Nepenthes. Insect N contributed 76.4 ± 8.4% (range 57–90%) to total pitcher N content. The data suggest complex patterns of partitioning of insect and soil-derived N between source and sink regions in pitcher plants and possibly higher dependence on insect N than recorded elsewhere for Drosera species. Received: 14 April 1997 / Accepted: 18 August 1997     

15N natural abundances and N use by tundra plants

Plant species collected from tundra ecosystems located along a north-south transect from central Alaska to the north coast of Alaska showed large and consistent differences in ¹⁵N natural abundances. Foliar ¹⁵N values varied by about 10% among species within each of two moist tussock tundra sites. Differences in ¹⁵N contents among species or plant groups were consistent across moist tussock tundra at several other sites and across five other tundra types at a single site. Ericaceous species had the lowest ¹⁵N values, ranging between about –8 to –6. Foliar ¹⁵N contents increased progressively in birch, willows and sedges to maximum ¹⁵N values of about +2 in sedges. Soil ¹⁵N contents in tundra ecosystems at our two most intensively studied sites increased with depth and ¹⁵N values were usually higher for soils than for plants. Isotopic fractionations during soil N transformations and possibly during plant N uptake could lead to observed differences in ¹⁵N contents among plant species and between plants and soils. Patterns of variation in ¹⁵N content among species indicate that tundra plants acquire nitrogen in extremely nutrient-poor environments by competitive partitioning of the overall N pool. Differences in plant N sources, rooting depth, mycorrhizal associations, forms of N taken up, and other factors controlling plant N uptake are possible causes of variations in ¹⁵N values of tundra plant species.     

Ecosystem N Distribution and δ<Superscript>15</Superscript>N during a Century of Forest Regrowth after Agricultural Abandonment

Abstract Stable isotope ratios of terrestrial ecosystem nitrogen (N) pools reflect internal processes and input–output balances. Disturbance generally increases N cycling and loss, yet few studies have examined ecosystem δ¹⁵N over a disturbance-recovery sequence. We used a chronosequence approach to examine N distribution and δ¹⁵N during forest regrowth after agricultural abandonment. Site ages ranged from 10 to 115 years, with similar soils, climate, land-use history, and overstory vegetation (white pine Pinus strobus). Foliar N and δ¹⁵N decreased as stands aged, consistent with a progressive tightening of the N cycle during forest regrowth on agricultural lands. Over time, foliar δ¹⁵N became more negative, indicating increased fractionation along the mineralization–mycorrhizal–plant uptake pathway. Total ecosystem N was constant across the chronosequence, but substantial internal N redistribution occurred from the mineral soil to plants and litter over 115 years (>25% of ecosystem N or 1,610 kg ha⁻¹). Temporal trends in soil δ¹⁵N generally reflected a redistribution of depleted N from the mineral soil to the developing O horizon. Although plants and soil δ¹⁵N are coupled over millennial time scales of ecosystem development, our observed divergence between plants and soil suggests that they can be uncoupled during the disturbance-regrowth sequence. The approximate 2‰ decrease in ecosystem δ¹⁵N over the century scale suggests significant incorporation of atmospheric N, which was not detected by traditional ecosystem N accounting. Consideration of temporal trends and disturbance legacies can improve our understanding of the influence of broader factors such as climate or N deposition on ecosystem N balances and δ¹⁵N. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Consequence of salinity and excess boron on growth, evapotranspiration and ion uptake in date palm (Phoenix dactylifera L., cv. Medjool)

Patches of common juniper (Juniperus communis L.) shrubs potentially facilitate the formation of fertile islands in heath tundra ecosystems thereby influencing the long-term resilience of these ecosystems. Although the role of juniper in the formation of such ‘islands of fertility’ has been studied in semiarid landscapes, there has been little attention paid to the importance of juniper in other ecosystems. In this study we contrast the soil fertility and rates of N fixation under juniper shrubs with that in open heath tundra in northern Sweden. Plots were established at several individual sites in alpine heath tundra in Northern Sweden and mineral soils to a depth of 10 cm were characterized for available N and P and total C, N, P, Ca, Mg, K, Fe, Mn, Zn, and Cu. Nitrogen fixation rates were measured by acetylene reduction in feather mosses under juniper canopies and contrasted with N fixation in both feather mosses and surface soils in the open heath. Soils under juniper had concentrations of total P greatly in excess of P in open heath, furthermore, juniper islands had the highest concentrations of bioavailable P. Nitrogen fixation rates in the feather moss Pleurozium schreberi (Bird.) Mitt were approximately 150 μmol acetylene reduced m⁻² d⁻¹ under the juniper canopy compared to less than 10 μmol acetylene reduced m⁻² d⁻¹ in the open heath. Feather mosses under the juniper canopy also fixed N at a significantly higher rate (on an aerial basis) than that of surface cores from the open heath that included lichen, mosses, and soil crusts. Juniper facilitates the formation of islands of soil fertility that may in turn facilitate the growth of other plants and positively influence the long term recovery of heath tundra ecosystems following disturbance.     

Changes in stable isotopic signatures of soil nitrogen and carbon during 40 years of forest development

Understanding what governs patterns of soil δ¹⁵N and δ¹³C is limited by the absence of these data assembled throughout the development of individual ecosystems. These patterns are important because stable isotopes of soil organic N and C are integrative indicators of biogeochemical processing of soil organic matter. We examined δ¹⁵N of soil organic matter (δ¹⁵N_SOM) and δ¹³C_SOM of archived soil samples across four decades from four depths of an aggrading forest in southeastern USA. The site supports an old-field pine forest in which the N cycle is affected by former agricultural fertilization, massive accumulation of soil N by aggrading trees over four decades, and small to insignificant fluxes of N via NH₃ volatilization, nitrification, and denitrification. We examine isotopic data and the N and C dynamics of this ecosystem to evaluate mechanisms driving isotopic shifts over time. With forest development, δ¹³C_SOM became depth-dependent. This trend resulted from a decline of ~2‰ in the surficial 15 cm of mineral soil to −26.0‰, due to organic matter inputs from forest vegetation. Deeper layers exhibited relatively little trend in δ¹³C_SOM with time. In contrast, δ¹⁵N_SOM was most dynamic in deeper layers. During the four decades of forest development, the deepest layer (35–60 cm) reached a maximum δ¹⁵N value of 9.1‰, increasing by 7.6‰. The transfer of >800 kg ha⁻¹ of soil organic N into aggrading vegetation and the forest floor and the apparent large proportion of ectomycorrhizal (ECM) fungi in these soils suggest that fractionation via microbial transformations must be the major process changing δ¹⁵N in these soils. Accretion of isotopically enriched compounds derived from microbial cells (i.e., ECM fungi) likely promote isotopic enrichment of soils over time. The work indicates the rapid rate at which ecosystem development can impart δ¹⁵N_SOM and δ¹³C_SOM signatures associated with undisturbed soil profiles.     

Depleted 15N in hydrolysable-N of arctic soils and its implication for mycorrhizal fungi–plant interaction

Uptake of nitrogen (N) via root-mycorrhizal associations accounts for a significant portion of total N supply to many vascular plants. Using stable isotope ratios (δ¹⁵N) and the mass balance among N pools of plants, fungal tissues, and soils, a number of efforts have been made in recent years to quantify the flux of N from mycorrhizal fungi to host plants. Current estimates of this flux for arctic tundra ecosystems rely on the untested assumption that the δ¹⁵N of labile organic N taken up by the fungi is approximately the same as the δ¹⁵N of bulk soil. We report here hydrolysable amino acids are more depleted in ¹⁵N relative to hydrolysable ammonium and amino sugars in arctic tundra soils near Toolik Lake, Alaska, USA. We demonstrate, using a case study, that recognizing the depletion in ¹⁵N for hydrolysable amino acids (δ¹⁵N = ?5.6‰ on average) would alter recent estimates of N flux between mycorrhizal fungi and host plants in an arctic tundra ecosystem.     

Nitrogen transfer between herbivores and their forage species

Herbivores may increase the productivity of forage plants; however, this depends on the return of nutrients from faeces to the forage plants. The aim of this study was to test if nitrogen (N) from faeces is available to forage plants and whether the return of nutrients differs between plant species using ¹⁵N natural abundance in faeces and plant tissue. To investigate the effect of grazing on N transfer, we carried out a grazing experiment in wet and mesic tundra on high Arctic Spitsbergen using barnacle geese (Branta leucopsis) as the model herbivore. N inputs (from faeces) increased with grazing pressure at both the wet and mesic sites, with the greatest N input from faeces at the wet site. The δ¹⁵N ratio in plant tissue from grazed plots was enriched in mosses and the dwarf shrub species, reflecting the δ¹⁵N signature of faeces-derived N, but no such pattern was observed in the dominant grasses. This study demonstrates that the δ¹⁵N signature of faeces and forage species is a useful tool to explore how grazing impacts on N acquisition. Our findings suggest that plant species which acquire their N close to the soil surface (e.g. mosses) access more of the N from faeces than species with deeper root systems (e.g. grasses) suggesting a transfer of N from the preferred forage species to the mosses and dwarf shrubs, which are less preferred by the geese. In conclusion, the moss layer appears to disrupt the nitrogen return from herbivores to their forage species.     

Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence

The successful use of natural abundances of carbon (C) and nitrogen (N) isotopes in the study of ecosystem dynamics suggests that isotopic measurements could yield new insights into the role of fungi in nitrogen and carbon cycling. Sporocarps of mycorrhizal and saprotrophic fungi, vegetation, and soils were collected in young, deciduous-dominated sites and older, coniferous-dominated sites along a successional sequence at Glacier Bay National Park, Alaska. Mycorrhizal fungi had consistently higher δ¹⁵N and lower δ¹³C values than saprotrophic fungi. Foliar δ¹³C values were always isotopically depleted relative to both fungal types. Foliar δ¹⁵N values were usually, but not always, more depleted than those in saprotrophic fungi, and were consistently more depleted than in mycorrhizal fungi. We hypothesize that an apparent isotopic fractionation by mycorrhizal fungi during the transfer of nitrogen to plants may be attributed to enzymatic reactions within the fungi producing isotopically depleted amino acids, which are subsequently passed on to plant symbionts. An increasing difference between soil mineral nitrogen δ¹⁵N and foliar δ¹⁵N in later succession might therefore be a consequence of greater reliance on mycorrhizal symbionts for nitrogen supply under nitrogen-limited conditions. Carbon signatures of mycorrhizal fungi may be more enriched than those of foliage because the fungi use isotopically enriched photosynthate such as simple sugars, in contrast to the mixture of compounds present in leaves. In addition, some ¹³C fractionation may occur during transport processes from leaves to roots, and during fungal chitin biosynthesis. Stable isotopes have the potential to help clarify the role of fungi in ecosystem processes. Received: 7 January 1998 / Accepted: 9 November 1998     

Subantarctic Macquarie Island – a model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance

Plants collected from diverse sites on subantarctic Macquarie Island varied by up to 30‰ in their leaf δ¹⁵N values. ¹⁵N natural abundance of plants, soils, animal excrement and atmospheric ammonia suggest that the majority of nitrogen utilised by plants growing in the vicinity of animal colonies or burrows is animal-derived. Plants growing near scavengers and animal higher in the food chain had highly enriched δ¹⁵N values (mean = 12.9‰), reflecting the highly enriched signature of these animals' excrement, while plants growing near nesting penguins and albatross, which have an intermediate food chain position, had less enriched δ¹⁵N values (>6‰). Vegetation in areas affected by rabbits had lower δ¹⁵N values (mean = 1.2‰), while the highly depleted δ¹⁵N values (below −5‰) of plants at upland plateau sites inland of penguin colonies, suggested that a portion of their nitrogen is derived from ammonia (mean ¹⁵N =−10‰) lost during the degradation of penguin guano. Vegetation in a remote area had δ¹⁵N values near −2‰. These results contrast with arctic and subarctic studies that attribute large variations in plant ¹⁵N values to nitrogen partitioning in nitrogen-limited environments. Here, plant ¹⁵N reflects the ¹⁵N of the likely nitrogen sources utilised by plants. Received: 18 December 1997 / Accepted: 13 June 1998