Alkaline air: changing perspectives on nitrogen and air pollution in an ammonia-rich world.

Ammonia and ammonium have received less attention than other forms of air pollution, with limited progress in controlling emissions at UK, European and global scales. By contrast, these compounds have been of significant past interest to science and society, the recollection of which can inform future strategies. Sal ammoniac (nushadir, nao sha) is found to have been extremely valuable in long-distance trade (ca AD 600-1150) from Egypt and China, where 6-8 kg N could purchase a human life, while air pollution associated with nushadir collection was attributed to this nitrogen form. Ammonia was one of the keys to alchemy-seen as an early experimental mesocosm to understand the world-and later became of interest as 'alkaline air' within the eighteenth century development of pneumatic chemistry. The same economic, chemical and environmental properties are found to make ammonia and ammonium of huge relevance today. Successful control of acidifying SO2 and NOx emissions leaves atmospheric NH3 in excess in many areas, contributing to particulate matter (PM2.5) formation, while leading to a new significance of alkaline air, with adverse impacts on natural ecosystems. Investigations of epiphytic lichens and bog ecosystems show how the alkalinity effect of NH3 may explain its having three to five times the adverse effect of ammonium and nitrate, respectively. It is concluded that future air pollution policy should no longer neglect ammonia. Progress is likely to be mobilized by emphasizing the lost economic value of global N emissions ($200 billion yr-1), as part of developing the circular economy for sustainable nitrogen management. This article is part of a discussion meeting issue 'Air quality, past present and future'.

Long-term interactive effects of N addition with P and K availability on N status of Sphagnum.

Little information exists concerning the long-term interactive effect of nitrogen (N) addition with phosphorus (P) and potassium (K) on Sphagnum N status. This study was conducted as part of a long-term N manipulation on Whim bog in south Scotland to evaluate the long-term alleviation effects of phosphorus (P) and potassium (K) on N saturation of Sphagnum (S. capillifolium). On this ombrotrophic peatland, where ambient deposition was 8 kg N ha-1 yr-1, 56 kg N ha-1 yr-1 of either ammonium (NH4+, Nred) or nitrate (NO3-, Nox) with and without P and K, were added over 11 years. Nutrient concentrations of Sphagnum stem and capitulum, and pore water quality of the Sphagnum layer were assessed. The N-saturated Sphagnum caused by long-term (11 years) and high doses (56 kg N ha-1 yr-1) of reduced N was not completely ameliorated by P and K addition; N concentrations in Sphagnum capitula for Nred 56 PK were comparable with those for Nred 56, although N concentrations in Sphagnum stems for Nred 56 PK were lower than those for Nred 56. While dissolved inorganic nitrogen (DIN) concentrations in pore water for Nred 56 PK were not different from Nred 56, they were lower for Nox 56 PK than for Nox 56 whose stage of N saturation had not advanced compared to Nred 56. These results indicate that increasing P and K availability has only a limited amelioration effect on the N assimilation of Sphagnum at an advanced stage of N saturation. This study concluded that over the long-term P and K additions will not offset the N saturation of Sphagnum.

Effects of airborne ammonium and nitrate pollution strongly differ in peat bogs, but symbiotic nitrogen fixation remains unaffected.

Pristine bogs, peatlands in which vegetation is exclusively fed by rainwater (ombrotrophic), typically have a low atmospheric deposition of reactive nitrogen (N) (<0.5kgha-1y-1). An important additional N source is N2 fixation by symbiotic microorganisms (diazotrophs) in peat and mosses. Although the effects of increased total airborne N by anthropogenic emissions on bog vegetation are well documented, the important question remains how different N forms (ammonium, NH4+, versus nitrate, NO3-) affect N cycling, as their relative contribution to the total load strongly varies among regions globally. Here, we studied the effects of 11years of experimentally increased deposition (32 versus 8kgNha-1y-1) of either NH4+ or NO3- on N accumulation in three moss and one lichen species (Sphagnum capillifolium, S. papillosum, Pleurozium schreberi and Cladonia portentosa), N2 fixation rates of their symbionts, and potential N losses to peat soil and atmosphere, in a bog in Scotland. Increased input of both N forms led to 15-90% increase in N content for all moss species, without affecting their cover. The keystone species S. capillifolium showed 4 times higher N allocation into free amino acids, indicating N stress, but only in response to increased NH4+. In contrast, NO3- addition resulted in enhanced peat N mineralization linked to microbial NO3- reduction, increasing soil pH, N concentrations and N losses via denitrification. Unexpectedly, increased deposition from 8 to 32kgha-1y-1 in both N forms did not affect N2 fixation rates for any of the moss species and corresponded to an additional input of 5kgNha-1y-1 with a 100% S. capillifolium cover. Since both N forms clearly show differential effects on living Sphagnum and biogeochemical processes in the underlying peat, N form should be included in the assessment of the effects of N pollution on peatlands.

The cost of surviving nitrogen excess: energy and protein demand in the lichen Cladonia portentosa as revealed by proteomic analysis.

MAIN CONCLUSION: Different nitrogen forms affect different metabolic pathways in lichens. In particular, the most relevant changes in protein expression were observed in the fungal partner, with NO 3- mostly affecting the energetic metabolism and NH 4+ affecting transport and regulation of proteins and the energetic metabolism much more than NO 3- did. Excess deposition of reactive nitrogen is a well-known agent of stress for lichens, but which symbiont is most affected and how, remains a mystery. Using proteomics can expand our understanding of stress effects on lichens. We investigated the effects of different doses and forms of reactive nitrogen, with and without supplementary phosphorus and potassium, on the proteome of the lichen Cladonia portentosa growing in a 'real-world' simulation of nitrogen deposition. Protein expression changed with the nitrogen treatments but mostly in the fungal partner, with NO3- mainly affecting the energetic metabolism and NH4+ also affecting the protein synthesis machinery. The photobiont mainly responded overexpressing proteins involved in energy production. This suggests that in response to nitrogen stress, the photobiont mainly supports the defensive mechanisms initiated by the mycobiont with an increased energy production. Such surplus energy is then used by the cell to maintain functionality in the presence of NO3-, while a futile cycle of protein production can be hypothesized to be induced by NH4+ excess. External supply of potassium and phosphorus influenced differently the responses of particular enzymes, likely reflecting the many processes in which potassium exerts a regulatory function.

Sphagnum can 'filter' N deposition, but effects on the plant and pore water depend on the N form.

The ability of Sphagnum moss to efficiently intercept atmospheric nitrogen (N) has been assumed to be vulnerable to increased N deposition. However, the proposed critical load (20kgNha(-1)yr(-1)) to exceed the capacity of the Sphagnum N filter has not been confirmed. A long-term (11years) and realistic N manipulation on Whim bog was used to study the N filter function of Sphagnum (Sphagnum capillifolium) in response to increased wet N deposition. On this ombrotrophic peatland where ambient deposition was 8kgNha(-1)yr(-1), an additional 8, 24, and 56kgNha(-1)yr(-1) of either ammonium (NH4(+)) or nitrate (NO3(-)) has been applied for 11years. Nutrient status of Sphagnum and pore water quality from the Sphagnum layer were assessed. The N filter function of Sphagnum was still active up to 32kgNha(-1)yr(-1) even after 11years. N saturation of Sphagnum and subsequent increases in dissolved inorganic N (DIN) concentration in pore water occurred only for 56kgNha(-1)yr(-1) of NH4(+) addition. These results indicate that the Sphagnum N filter is more resilient to wet N deposition than previously inferred. However, functionality will be more compromised when NH4(+) dominates wet deposition for high inputs (56kgNha(-1)yr(-1)). The N filter function in response to NO3(-) uptake increased the concentration of dissolved organic N (DON) and associated organic anions in pore water. NH4(+) uptake increased the concentration of base cations and hydrogen ions in pore water though ion exchange. The resilience of the Sphagnum N filter can explain the reported small magnitude of species change in the Whim bog ecosystem exposed to wet N deposition. However, changes in the leaching substances, arising from the assimilation of NO3(-) and NH4(+), may lead to species change.

Evidence for differential effects of reduced and oxidised nitrogen deposition on vegetation independent of nitrogen load.

Nitrogen (N) deposition impacts natural and semi-natural ecosystems globally. The responses of vegetation to N deposition may, however, differ strongly between habitats and may be mediated by the form of N. Although much attention has been focused on the impact of total N deposition, the effects of reduced and oxidised N, independent of the total N deposition, have received less attention. In this paper, we present new analyses of national monitoring data in the UK to provide an extensive evaluation of whether there are differences in the effects of reduced and oxidised N deposition across eight habitat types (acid, calcareous and mesotrophic grasslands, upland and lowland heaths, bogs and mires, base-rich mires, woodlands). We analysed data from 6860 plots in the British Countryside Survey 2007 for effects of total N deposition and N form on species richness, Ellenberg N values and grass:forb ratio. Our results provide clear evidence that N deposition affects species richness in all habitats except base-rich mires, after factoring out correlated explanatory variables (climate and sulphur deposition). In addition, the form of N in deposition appears important for the biodiversity of grasslands and woodlands but not mires and heaths. Ellenberg N increased more in relation to NHx deposition than NOy deposition in all but one habitat type. Relationships between species richness and N form were habitat-specific: acid and mesotrophic grasslands appear more sensitive to NHx deposition while calcareous grasslands and woodlands appeared more responsive to NOy deposition. These relationships are likely driven by the preferences of the component plant species for oxidised or reduced forms of N, rather than by soil acidification.

Inertia in an ombrotrophic bog ecosystem in response to 9 years' realistic perturbation by wet deposition of nitrogen, separated by form.

Wet deposition of nitrogen (N) occurs in oxidized (nitrate) and reduced (ammonium) forms. Whether one form drives vegetation change more than the other is widely debated, as field evidence has been lacking. We are manipulating N form in wet deposition to an ombrotrophic bog, Whim (Scottish Borders), and here report nine years of results. Ammonium and nitrate were provided in rainwater spray as NH4 Cl or NaNO3 at 8, 24 or 56 kg N ha(-1)  yr(-1) , plus a rainwater only control, via an automated system coupled to site meteorology. Detrimental N effects were observed in sensitive nonvascular plant species, with higher cumulative N loads leading to more damage at lower annual doses. Cover responses to N addition, both in relation to form and dose, were species specific and mostly dependent on N dose. Some species were generally indifferent to N form and dose, while others were dose sensitive. Calluna vulgaris showed a preference for higher N doses as ammonium N and Hypnum jutlandicum for nitrate N. However, after 9 years, the magnitude of change from wet deposited N on overall species cover is small, indicating only a slow decline in key species. Nitrogen treatment effects on soil N availability were likewise small and rarely correlated with species cover. Ammonium caused most N accumulation and damage to sensitive species at lower N loads, but toxic effects also occurred with nitrate. However, because different species respond differently to N form, setting of ecosystem level critical loads by N form is challenging. We recommend implementing the lowest value of the critical load range where communities include sensitive nonvascular plants and where ammonium dominates wet deposition chemistry. In the context of parallel assessment at the same site, N treatments for wet deposition showed overall much smaller effects than corresponding inputs of dry deposition as ammonia.

The global nitrogen cycle in the twenty-first century.

Global nitrogen fixation contributes 413 Tg of reactive nitrogen (Nr) to terrestrial and marine ecosystems annually of which anthropogenic activities are responsible for half, 210 Tg N. The majority of the transformations of anthropogenic Nr are on land (240 Tg N yr(-1)) within soils and vegetation where reduced Nr contributes most of the input through the use of fertilizer nitrogen in agriculture. Leakages from the use of fertilizer Nr contribute to nitrate (NO3(-)) in drainage waters from agricultural land and emissions of trace Nr compounds to the atmosphere. Emissions, mainly of ammonia (NH3) from land together with combustion related emissions of nitrogen oxides (NOx), contribute 100 Tg N yr(-1) to the atmosphere, which are transported between countries and processed within the atmosphere, generating secondary pollutants, including ozone and other photochemical oxidants and aerosols, especially ammonium nitrate (NH4NO3) and ammonium sulfate (NH4)2SO4. Leaching and riverine transport of NO3 contribute 40-70 Tg N yr(-1) to coastal waters and the open ocean, which together with the 30 Tg input to oceans from atmospheric deposition combine with marine biological nitrogen fixation (140 Tg N yr(-1)) to double the ocean processing of Nr. Some of the marine Nr is buried in sediments, the remainder being denitrified back to the atmosphere as N2 or N2O. The marine processing is of a similar magnitude to that in terrestrial soils and vegetation, but has a larger fraction of natural origin. The lifetime of Nr in the atmosphere, with the exception of N2O, is only a few weeks, while in terrestrial ecosystems, with the exception of peatlands (where it can be 10(2)-10(3) years), the lifetime is a few decades. In the ocean, the lifetime of Nr is less well known but seems to be longer than in terrestrial ecosystems and may represent an important long-term source of N2O that will respond very slowly to control measures on the sources of Nr from which it is produced.

Methane indicator values for peatlands: a comparison of species and functional groups.

Previous studies have shown a correspondence between the abundance of particular plant species and methane flux. Here, we apply multivariate analyses, and weighted averaging, to assess the suitability of vegetation composition as a predictor of methane flux. We developed a functional classification of the vegetation, in terms of a number of plant traits expected to influence methane production and transport, and compared this with a purely taxonomic classification at species level and higher. We applied weighted averaging and indirect and direct ordination approaches to six sites in the United Kingdom, and found good relationships between methane flux and vegetation composition (classified both taxonomically and functionally). Plant species and functional groups also showed meaningful responses to management and experimental treatments. In addition to the United Kingdom, we applied the functional group classification across different geographical regions (Canada and the Netherlands) to assess the generality of the method. Again, the relationship appeared good at the site level, suggesting some general applicability of the functional classification. The method seems to have the potential for incorporation into large-scale (national) greenhouse gas accounting programmes (in relation to peatland condition/management) using vegetation mapping schemes. The results presented here strongly suggest that robust predictive models can be derived using plant species data (for use in national-scale studies). For trans-national-scale studies, where the taxonomic assemblage of vegetation differs widely between study sites, a functional classification of plant species data provides an appropriate basis for predictive models of methane flux.

Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment.

We review the ecological consequences of N deposition on the five Mediterranean regions of the world. Seasonality of precipitation and fires regulate the N cycle in these water-limited ecosystems, where dry N deposition dominates. Nitrogen accumulation in soils and on plant surfaces results in peaks of availability with the first winter rains. Decoupling between N flushes and plant demand promotes losses via leaching and gas emissions. Differences in P availability may control the response to N inputs and susceptibility to exotic plant invasion. Invasive grasses accumulate as fuel during the dry season, altering fire regimes. California and the Mediterranean Basin are the most threatened by N deposition; however, there is limited evidence for N deposition impacts outside of California. Consequently, more research is needed to determine critical loads for each region and vegetation type based on the most sensitive elements, such as changes in lichen species composition and N cycling.

Direct and indirect effects of ammonia, ammonium and nitrate on phosphatase activity and carbon fluxes from decomposing litter in peatland.

Here we investigate the response of soils and litter to 5 years of experimental additions of ammonium (NH4), nitrate (NO3), and ammonia (NH3) to an ombrotrophic peatland. We test the importance of direct (via soil) and indirect (via litter) effects on phosphatase activity and efflux of CO2. We also determined how species representing different functional types responded to the nitrogen treatments. Our results demonstrate that additions of NO3, NH4 and NH3 all stimulated phosphatase activity but the effects were dependent on species of litter and mechanism (direct or indirect). Deposition of NH3 had no effect on efflux of CO2 from Calluna vulgaris litter, despite it showing signs of stress in the field, whereas both NO3 and NH4 reduced CO2 fluxes. Our results show that the collective impacts on peatlands of the three principal forms of nitrogen in atmospheric deposition are a result of differential effects and mechanisms on individual components.

Stress responses of Calluna vulgaris to reduced and oxidised N applied under 'real world conditions'.

Effects and implications of reduced and oxidised N, applied under 'real world' conditions, since May 2002, are reported for Calluna growing on an ombrotrophic bog. Ammonia has been released from a 10 m line source generating monthly concentrations of 180-6 microg m(-3), while ammonium chloride and sodium nitrate are applied in rainwater at nitrate and ammonium concentrations below 4mM and providing up to 56 kg N ha(-1) year(-1) above a background deposition of 10 kg N ha(-1) year(-1). Ammonia concentrations, >8 microg m(-3) have significantly enhanced foliar N concentrations, increased sensitivity to drought, frost and winter desiccation, spring frost damage and increased the incidence of pathogen outbreaks. The mature Calluna bushes nearest the NH3 source have turned bleached and moribund. By comparison the Calluna receiving reduced and oxidised N in rain has shown no significant visible or stress related effects with no significant increase in N status.

Causal mechanisms by which sulphate, nitrate and acidity influence frost hardiness in red spruce: review and hypothesis.

This paper summarizes results from four experiments in which red spruce seedlings (Picea rubens Sarg.) were exposed to simulated acid mist containing SO4 2- , NH4- , NO3 - and H+ ions. Seedlings were grown in compost, with or without fertilizer, in charcoal filtered air in open-top chambers near Edinburgh, Scotland. Plants were sprayed from bud burst between May and November with mist containing different concentrations and combinations of the four major ions to provide a range of doses, which were applied at different frequencies. Reductions in frost hardiness expressed in terms of the temperature which killed 50% of shoots (LT50 ) were significantly correlated with the dose of S received by the seedlings. Differences in foliar S concentrations between the controls and treated plants were correlated with S dose. Absolute S concentrations were, however, of limited use for predictive purposes. Seedlings appear to be more sensitive than older trees to S toxicity because the former have the greatest proportion of newly expanding needles which optimize conditions for foliar uptake. Seedlings are also least well equipped to export SO4 2- ions since they have a smaller resource of older foliage to supplement their assimilate pool. In conditions which promote uncontrolled SO4 2- ion uptake by foliage, i.e. high external SO4 2- concentrations and incompletely formed cuticles, the potential exists for the internal build up of SO4 2- ions. It is proposed that in the absence of sufficient assimilate and K the presence of these high concentrations of SO4 2- ions in the apoplast or cytosol can lead to protein denaturation and loss of membrane integrity. Reductions in frost hardiness appear to result through direct attack by SO4 2 ions on membrane proteins which impairs their function. Indirect effects on hardiness occur through both an increased consumption of sugars reducing the'pool'available for cryoprotection and a reduction in photosynthetic function, the ability to produce sugars. The presence of NO3- N mitigates the toxic effects of SO4 2 because SO4 2 ions are consumed in assimilation processes which both utilize and are facilitated by the presence of large amounts of fertilizer N. High concentrations of SO4 2 and H+ are found to be particularly toxic because of the synergistic effects these ions exert on their mutual uptake with devastating consequences for the control of cellular pH. Trees growing at high altitude sites are likely to be particularly sensitive to SO4 2- toxicity because (1) their carbon balance is low, (2) cuticle development is poor and (3) levels of soil available Ca2 tend to be low relative to Al3+ so that membranes may already be weakened as a result of insufficient Ca2+ ions for protein bridging.

Influence of acidic mist on frost hardiness and nutrient concentrations in red spruce seedlings: 1. Exposure of the foliage and the rooting environment.

Two-year-old red spruce (Picea rubens Sarg.) was grown in replicated open-top chambers supplied with charcoal-filtered air near Edinburgh, Scotland. Between May and November 1989, plants were exposed to four mist treatments, three containing sulphuric acid and ammonium nitrate in equimolar concentrations at 0.005 mol m-3 (pH 5) or 1.0 mol m-3 (pH 27), and a fourth treatment with sulphuric acid alone at 1.0 mol m3 (equivalent to 2 mm precipitation). Two dose rates were used for the pH 2.7 treatment equivalent to 2 and 8 mm of rain per week. Three subtreatments (soil surface exposed to mist, addition of extra sulphuric acid to the soil surface, exclusion of mist from the soil) were included in each chamber. Frost hardiness was assessed by measuring rates of electrolyte leakage after controlled freezing of detached shoots. At the end of October, frost hardiness, expressed as the lethal temperature for 50% of shoots (LT50 ), was decreased by 8 °C in the 8 mm wk-1 treatment at pH 27, compared to pH 5. The 2 mm wk-1 treatment at pH 2.7 had no effect on frost hardiness either when ammonium nitrate was present or absent (i.e. sulphuric acid only). Excluding mist from the soil, and adding extra sulphuric acid, both increased frost hardiness by about 3 °C when compared with uncovered soil. Excluding mist from the soil increased the amount of foliage initiated and produced inside the chambers but neither subtreatment, excluding the mist nor providing additional sulphuric acid to the soil affected foliar nutrient concentrations. Mist of pH 27 as sulphuric acid alone and in combination with ammonium nitrate both enhanced N uptake. Several observations concerning the effect of acidic mist on frost hardiness were confirmed by this study: (i) preventing mist from reaching the soil/roots, improving conditions for root growth can ameliorate the effects of acidic mist on shoot growth and frost hardiness; (ii) the effect was determined by the ion dose but not by the ion concentration in the mist; (iii) the effect was primarily mediated through foliar absorption; (iv) the presence of high foliar nitrogen concentrations did not increase frost hardiness when foliar sulphur concentrations were also high; (v) low N concentrations were more important for frost hardiness than high foliar N concentrations.

Influence of acidic mist on frost hardiness and nutrient concentrations in red spruce seedlings: 2. Effects of misting frequency and rainfall exclusion.

Two-year-old red spruce (Picea rubens Sarg.) of Pittston provenance and 3-yr-old plants of Chatham provenance were exposed to acid mist in replicated open-top chambers supplied with charcoal-filtered air near Edinburgh, Scotland. Plants of Chatham provenance had already been exposed to acid mist throughout the previous growing season. The plants were exposed to mist, equivalent to 4 mm rainfall per week, containing an equimolar mixture of sulphuric acid and ammonium nitrate at pH 2.5 or pH 5.0 (1.6 or 0.01 mol m3 ) from May to November. This weekly dose was delivered at a low frequency (2 mm twice a week), or high frequency (1 mm on 4 consecutive days each week) to chambers fitted with ceilings to exclude rain. The low frequency dose was also applied to chambers without ceilings, to examine the effect of natural washing by rain. Frost hardiness, estimated by exposing detached shoots to controlled freezing and then measuring rates of electrolyte leakage, was determined during the misting period at the end of October and in December. Foliar nutrient concentrations were measured during the dormant period after treatment had ceased. At the end of October, plants which had received acid mist were less frost hardy than plants receiving mist at pH 5. The temperature causing 50% shoot death (LT50 ) increased by 6 °C for low frequency application, and by 10 °C at high frequency, relative to the plants receiving mist at pH 5. Exclusion of ambient rainfall had no detectable effect on the frost hardiness response to acid mist. In December, 3 wk after the cessation of misting, all plants were more frost hardy than in October. Significant effects of the acid mist treatment could no longer be detected. Differences in nutrient concentrations were small among treatments, although K+ concentrations in the low frequency treatment with acid mist with rain exclusion were 50 % below those in other treatments. Ca concentrations were 50% larger in the acid mist treatment with rain exclusion than without. The data suggested enhanced sulphate uptake resulting from increasing the frequency of exposure, but the increase was not significant. There was no clear relationship between the pattern of frost hardiness and nutrient concentrations except for S, which was 30% smaller in the control plants (pH 5) than in the high frequency pH 2.5 treatments. It is concluded that excluding rainfall, an experimental artifact introduced in evaluating effects of acid mist, does not influence the frost hardiness response of red spruce seedlings. The much greater effect of exposure to the same dose at double the frequency suggests that such experiments may underestimate effects in the field, if those trees are exposed to more frequent episodes of polluted cloud water than experimental plants.