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

royalsocietypublishing.org/journal/rsta Research Cite this article: Sutton MA et al.2020 Alkaline air: changing perspectives on nitrogen and air pollution in an ammonia-rich world. Phil.Trans.R.Soc.A378: 20190315. http://dx.doi.org/10.1098/rsta.2019.0315 Accepted: 7 August 2020 One contribution of 17 to a discussion meeting issue ‘Air quality, past present and future’. Subject Areas: atmospheric chemistry, environmental chemistry, atmospheric science, biogeochemistry Keywords: alkaline air, nitrogen, n¯ ush¯ adir, lichens, ecosystem recovery, circular economy Author for correspondence: Mark A. Sutton e-mail: [email protected].uk Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare. c.5099293. Alkaline air: changing perspectives on nitrogen and air pollution in an ammonia-rich world Mark A. Sutton1,NettyvanDijk 1, Peter E. Levy1, Matthew R. Jones1, Ian D. Leith1,LucyJ.Sheppard 1, Sarah Leeson1,Y.SimTang 1, Amy Stephens1, Christine F. Braban1, Ulrike Dragosits1, Clare M. Howard1, Massimo Vieno1, David Fowler1, Paul Corbett2,Mohd Irfan Naikoo3, Silvana Munzi4,5, Christopher J. Ellis6, Sudipto Chatterjee7, Claudia E. Steadman1,8,Andrea Móring1,8 and Patricia A. Wolseley9 1UK Centre for Ecology & Hydrology, Edinburgh Research Station, Bush Estate, Penicuik, UK 2Northern Ireland Environment Agency, Belfast, UK 3Department of Botany, Aligarh Muslim University (AMU), Aligarh, India 4Centro Interuniversitário de História das Ciências e da Tecnologia, Faculdade de Ciências, Lisbon, Portugal 5Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Lisbon, Portugal 6Royal Botanic Garden Edinburgh (RBGE), Edinburgh, UK 7Department of Natural Resources, TERI School of Advanced Studies (TERISAS), New Delhi, India 8School of Geosciences, University of Edinburgh, Edinburgh, UK 9Natural History Museum, Cromwell Road, London, UK MAS, 0000-0002-1342-2072;DF,0000-0002-2999-2627 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 2020 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/ by/4.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 2 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... compounds have been of significant past interest to science and society, the recollection of which can inform future strategies. Sal ammoniac (n¯ ush¯ adir,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 n¯ ush¯ adir 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 SO2and NOxemissions leaves atmospheric NH3in 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 NH3may 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’. 1. Introduction Over recent decades ammonia (NH3) has often seemed like the Cinderella of air pollution, as it has been given much less attention than other pollutants, such as sulfur dioxide (SO2), nitrogen oxides (NOx), ozone (O3) and particulate matter (PM). In the 1980s, research focused on ‘acid rain’, especially in the light of SO2and NOxemissions [1–3]withonlyafewresearchersat that time examining the possible effects of NH3and ammonium (NH4+) on the environment, including threats to soils, biodiversity and forest health [4–6]. The same can be said for European air pollution policy, with successive international protocols on SO2and NOxemissions [7,8], preceding the multi-pollutant, multi-effect Gothenburg Protocol [9], which included NH3for the first time. Even then, the commitments for NH3were much less ambitious than for other air pollutants, requiring that little action be taken by most countries. The situation is similar with the 2020 ceilings of the revised Gothenburg Protocol of 2012. With insufficient measures implemented, several countries are unlikely to meet their legally binding NH3ceilings for 2020, while overall Europe-wide NH3emissions have actually been increasing since 2013 [10]. The barriers appear to be primarily political, as The Netherlands and Denmark have shown that it is possible to reduce NH3emissions substantially. With this perspective in mind, it is appropriate to take stock of what ammonia has meant to people in the past, what it means today, and what it might mean in the future. We rapidly discover that NH3and NH4+were historically far from insignificant, fulfilling several important roles. Whereas recent efforts have focused on reducing NH3emissions from agriculture, with the main sources being livestock excreta and fertilizers, the historical picture helps to raise awareness of the multi-dimensional relevance of ammonia for environment and society. Considering the present, across much of Europe and North America we now inherit a world where substantial emission controls have already been achieved for SO2and NOx.Weconsider in detail the implications of the changed ratio of NH3to the acid gases, especially for some of the most sensitive ecological receptors. Instead of acid rain, we now face challenges from ‘alkaline air’, which was the original name given by Joseph Priestley [11] for gaseous ammonia. Today, we may also define alkaline air more generally as air where alkaline gases (primarily NH3,butin principle also including volatile amines) dominate over those that are acidic in nature. Finally, we consider what might be expected for the future. What are the implications of current legislation, of the slightly more ambitious emission reductions for 2030 under the revised EU Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 3 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... National Emissions Ceilings Directive (2016/2284/EU)? We conclude by placing NH3mitigation in the context of the circular economy for nitrogen and United Nations actions on nitrogen to help meet multiple Sustainable Development Goals (SDGs). In the following sections, we show how a broad approach linking past, present and future could help raise awareness about the importance of ammonia and nitrogen as a contribution to catalysing action on the SDGs. We juxtapose the historical value of ammonium in international trade and alchemy with current development of the nitrogen circular economy. The analysis is underpinned with a more detailed examination of ecological datasets for epiphytic lichens and bog ecosystems which together emphasize the emerging importance of alkaline air. 2. Ammonia in the past and implications for the present While the popular historical narrative ascribes the discovery of ammonia to Priestley [11], his achievement needs to be set in the context of at least two millennia of human exploration and investigation into ammonia and ammonium. (a) Ammonia in ancient times By the start of the Tang Dynasty (AD 618–907), ammonium salts for use in metallurgy, medicine and food were already being traded as a luxury product along the Silk Road in Central Asia [12]. Spontaneous combustion of near-surface coal deposits explains the development of fire caves, some of which burn for hundreds of years. Nitrogen (N) in the burnt coal volatilizes as NH3, reacting with co-emitted hydrochloric acid (HCl), sulfuric acid (H2SO4) and nitric acid (HNO3) to form a mix of ammonium chloride, sulfate and nitrate salts [13]. Ammonium chloride tends to dominate in the collected sublimate (also known as n¯ ush¯ adir,nao sha, sal ammoniac, the Eagle (nasr) and a wealth of other names), presumably because it is more volatile than ammonium sulfate, while ammonium nitrate formation may be limited by low HNO3concentrations relative to NOx(ammonium nitrate is also decomposed to N2,N 2O and water at high temperatures). Along with many other point sources, NH3emissions from such fire caves can now be detected from space [14], such as at Jharia in India [10](figure 1). The historical collection of the sal ammoniac sublimate around the cooler edge of fire caves, as well as from a range of volcanic fumaroles (from Etna in Sicily to Mount Damavand in Iran), allowed it to become a key commodity of long-distance trade up to the early nineteenth century [12]. The importance and the stability of the sal ammoniac market can be illustrated by comparing prices from AD 620 (Central Asia) with those from AD 1000–1140 (Mediterranean trade) as shown in table 1. The estimates for Central Asia are based on transactions recorded in tax records discovered near Turfan, in present-day Xinjiang province of China [15]. These values are compared with documentary records recovered from a geniza or document repository, as uniquely preserved in Cairo [16]. Table 1 shows impressive similarity for the prices of sal ammoniac and spice from these independent datasets, while the price of silk and slaves had increased substantially in Cairo compared with Central Asia. With today’s perspective, it is shocking to note that just 6–8 kg N would purchase a human being. This reflects both a high price of nitrogen and a low value of human life compared with the present. Relative to changing gold and silver prices (electronic supplementary material, §2), N compounds are today around three orders of magnitude cheaper, with prices decreasing rapidly during the twentieth century as large-scale manufacture, mainly through the Haber–Bosch Process [17], has increased their availability. The burning coal caves of Central Asia also provide the first recorded example of ammoniacal air pollution. It appears that locals would encourage the natural coal burning specifically to harvest sal ammoniac, as recorded by ibn-Hauqal: Over the spot whence the vapour issues, they have erected a house, the doors and windows of which are kept so closely shut and plastered over with clay that none of the vapour can Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 4 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... Figure 1. Fire cave at Jharia, India, where spontaneous combustion of surface coal deposits has resulted in burning at this locationforoveracentury.SitessuchasthisacrossCentralAsia,togetherwithvolcanicfumaroles,representtheearliestrecorded sources of traded ammonium salts (Photo ©Johnny Haglund). (Online version in colour.) Table 1. Comparison of sal ammoniac prices with spice, silk and slaves for Central Asian and Mediterranean trade during the seventh and eleventh to twelveth centuries. For calculations, see electronic supplementary material, §1. prices in nuqra dirhams (pure silver dirhams, d)a location (main trade locations) date sal ammoniac (d/kg) spice (d/kg) silk (d/kg) slaves (d/slave) Ncostofa human (kg N/slave)b Turfan (China, Central Asia) ca 620 6c517120 6 .......................................................................................................................................................................................................... Egypt (Sicily, Tunisia) 1000–1140 7.6(5.9–10.6)d5 59 243 (208–278)d8.4 (5.7–11.1)d .......................................................................................................................................................................................................... aDerived from data for Turfan [15]andEgypt[16]. bConverted based on N content of sal ammoniac of 26.2%. cThe estimates for Turfan draw on six transactions for sal ammoniac, of which one includes the amount of tax paid, with a second combined transaction of sal ammoniac and spice that agrees within 10%. d95% confidence limits with n=12 and 19 for sal ammoniac and slave price, respectively. escape. On the upper part of this house the n¯ ush¯ adir rests. When the doors are to be opened, a swiftly running man is chosen, who having his body covered over with clay, opens the door; takes as much as he can of the n¯ ush¯ adir, and runs off; if he should delay, he would be burnt (translated by Ouseley [18], p. 264, who renders n¯ ush¯ adir as ‘copperas’). Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 5 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... Further details of the pollution threat are given by al-Mas’¯ ud¯ ı: Travellers in summer take their road from Khor¯ as¯ an to China by this mountain; for there is a valley through it, which is forty or fifty miles long. At the entrance of the valley wait some men who offer themselves to carry the baggage, if they are well paid. They use sticks to drive the passengers on their journey; for any stoppage or rest would be fatal to the traveller, in consequence of the irritation which the ammoniacal vapours of this valley produce on the brain, and on account of the heat. The way becomes more and more narrow till the travellers come to the end of their perilous passage. Here are pits with water, in which they throw themselves, to obtain relief ... When travellers arrive in the Chinese territories, they are beaten as in passing (to counteract the congestion of blood in the brain) (translated by Sprenger [19], pp. 359–360). Caution is needed with regard to the comment of al-Mas’¯ ud¯ ı about effects of n¯ ush¯ adir on the brain. This may reflect the fact that the Chinese term, nao sha, includes a component referring to the brain, so that nao sha was sometimes termed brain salt (see [20], pp. 446–447), for which there are several possible explanations. (b) Early ammonia science and philosophy While the above examples illustrate the historic importance of ammonium in trade and air pollution, these were probably not the earliest applications. Pliny the Elder (Natural History 28: 19, 149) was already familiar with use of the fumes of deer horn and hair to make people breathe naturally when choking with hysteria. This use is directly analogous to the eighteenth century popularity of ammonium carbonate as ‘smelling salts’; these liberate gaseous NH3, which acts as a vasodilator in the airways. Ammonia and ammonium were also known in scientific circles, if not always openly. In particular, they were at the heart of alchemy, well-known as a ‘reserved’ science (i.e. unspoken, secret, limited to the few), making it extremely difficult to trace how they were used. One of the most clear alchemical writers on n¯ ush¯ adir was the Persian physician al-R¯ az¯ ı. It has often been stated that earlier Greek alchemy used exclusively metals and other minerals, while Islamic alchemy introduced the use of organic materials (e.g. [20], p. 435, [21]). The following illustrates the methods of al-R¯ az¯ ı: Take of black cleaned hair, distil its water and oil and calcine its residue according to what is [explained] further above, and put away each part of it separately ... Then tie it [the solidified oil] up in a linen cloth and hang it into distilled urine in a clay container on the hook of the blind [cucurbit]. Place it on a small oven under which burns a fire of a lamp. Leave it for 24 h, that the urine becomes red. Then pour it off and renew the urine. Repeat this operation until all the colour is extracted. Then gather all and distil. Distil white urine, but its redness remains. Then mix that what remained from the oil in a batch with the distilled juice of a lemon and treat it with the urine with the help of the operation ... Then convert it into a hard state in a blind [cucurbit]; it solidifies it into white nuqra like crystal ... But if you want, that it [transmutes] into the red [into gold], thus put in it before it solidifies, the red [residue] ... it solidifies, transmuting into red nuqra,adirhamof which transmutes 1800 dirham of any metal whichever you want into pure gold (trans. by G. Fischer from [22], pp. 109–110). Special caution is needed here, as al-R¯ az¯ ı uses so-called ‘cover names’ (Decknamen), referring to the ammoniacal distillates as ‘urine’ (because of how it comes out of the alembic) or ‘lemon juice’ (because of its sharpness). Considering these processes, the Arab/Persian alchemist J¯ abir refers to alchemy as a mesocosm or middle-world, which links understanding of the macrocosm (universe) with the microcosm (humans) (cf. [23], p. 74). In experiments like this, ammonia and ammonium were key to early experimental philosophy. As to the gold, even more caution is needed. In the Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 6 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... margin of one manuscript, one of al-R¯ az¯ ı’s readers commented: ‘Truly I have looked into this book ... Do not occupy yourself with them [the essences of Arsenic and Sulphur] unless you already know the secret of the process ... Only if you know the secret, God willing, will you accomplish the work’ (translated by Heym [24], p. 191). In fact, it looks likely that earlier Greek alchemists were already familiar with ammonia and ammonium salts. For example, characteristic steps from the al-R¯ az¯ ı process given above can be found in writings of the Greek alchemist Zosimus (e.g. [25], pp. 30–33; [26], pp. 486–492) and in those attributed to Democritus (e.g. [27], p. S91; electronic supplementary material, §3). There is also a question about the oldest name for sal ammoniac. The term n¯ ush¯ adir appears earliest in its Chinese rendering as nao sha, but has a well-established Iranian etymology, meaning ‘immortal fire’ [12]. It is a name that matches just as well to the macrocosmic fire caves as to the processing of ‘elements’ in the mesocosmic analysis of earlier Greek alchemy, leaving open the question of its origin. Obscure as these beginnings may seem, they form the foundations on which modern science was built. This is no more apparent than with Isaac Newton, who experimented and wrote extensively on alchemy, but deliberately kept his findings secret (e.g. [28], p. 159) and encouraged others to do so. Newton thus wrote to Henry Oldenburg, the Secretary of the Royal Society, encouraging Robert Boyle not to reveal alchemical secrets: [It] may possibly be an inlet to something more noble, not to be communicated without immense dammage to ye world if there should be any verity in ye Hermetick writers, therefore I question not but that ye great wisdom of ye noble Authour [Boyle] will sway him to high silence till he shall be resolved of what consequence ye thing may be ... there being other things beside ye transmutation of metals ... which none but they [the alchemists] understand ... but pray keep this letter private to your self [29]. The message was the traditional one of many alchemists over the centuries: not to reveal the secrets of alchemy, which could otherwise lead to the destruction of society (cf. al-Jildak¯ ı[30], p. 49). While Boyle may have engaged in the practice of advertising secrecy [31], Newton appears to have recognized the ethical dilemma concerning open explanation of alchemy. (c) The discovery of ‘alkaline air’ Ultimately, the scientific community turned away from the secrecy of alchemy, pushing towards openness of scientific publication for practical benefit. As the experimentalist Stephen Hales wrote in the year that Newton died: If those who unhappily spent their time and substance in search after an imaginary production, that was to reduce all things to gold, had, instead of that fruitless pursuit, bestowed their labour in searching after this much neglected volatile Hermes, who has so often escaped thro’ their burst receivers, in the disguise of a subtile spirit, a mere explosive matter; they would then instead of reaping vanity, have found their researches rewarded with very considerable and useful discoveries ([32], p. 180). Hales’ experiments were to be decisive as a prelude to the scientific discovery of ammonia. His work introduced the idea of ‘pneumatic chemistry’, distilling all sorts of products and then collecting the resulting gases in an inverted vessel over a trough of water. In the case of ammonia distilled from blood or harts-horn, this first filled the vessel, but then gradually dissolved in the water, leaving Hales with no ammonia to collect (e.g. [32], p. 95, Experiment XLIX). Continuing these kinds of experiments 50 years later, Joseph Priestly instead filled his pneumatic trough with mercury in which the ammonia would not dissolve. This enabled him to isolate and characterize pure ammonia gas [11]. Priestley’s first report was in a private letter to Benjamin Franklin in September 1773, later presenting his findings to the Royal Society ([33], pp. 93–99). Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 7 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... It was only in the 1790s that Priestley’s alkaline air started to become known as ‘ammonia pura’, given its relationship to sal ammoniac. Subsequent chemical discoveries came quickly, with Scheele [34] showing that it was present in the atmosphere, and Berthellot [35] demonstrating that it consisted of one part nitrogen to three parts hydrogen. 3. Ammonia and present-day changes in air pollution climate The reminder of ammonia as alkaline air is highly relevant to the present, as emissions of SO2 and NOxhave decreased greatly over the last 30 years, leaving European and North American atmospheres increasingly rich in NH3. This can be illustrated by the temporal evolution of emissions, gas and aerosol concentrations and rainfall acidity across the UK. While SO2emissions have been almost entirely abated (97% reduction since 1970) and NOxemissions reduced by 70%, estimated NH3emissions increased substantially up to 1990, decreased by 18% (1990– 2013), and then increased 9% (2013–2017; figure 2a). National mean NH3concentrations have not changed significantly since the National Ammonia Monitoring Network [37] was started in 1997 (though increasing in remote areas), while aerosol NH4+concentrations have decreased significantly, consistent with declining SO2and HNO3(figure 2b). This has led to less formation of ammonium sulfate and ammonium nitrate, which will have also helped maintain gaseous NH3 levels [38,39]. As a consequence, acid rain is now a thing of the past for UK conditions. Since 1986, volumeweighted rain pH has increased from 4.62 to 5.48 (figure 2c), now being close to the value of 5.6 due to dissolution of atmospheric CO2. Together these changes demonstrate how alkaline air is becoming increasingly important across the UK countryside, in a pattern that is reflected across much of Europe and North America [40,41]. A corresponding trend is now occurring in China, following implementation of SO2emission controls from 2012 [42], while in India, NOx emissions have been increasing even faster than NH3emissions [43]. The gaseous alkaline fraction (expressed as NH3divided by the sum of NH3,2SO 2, HNO3and HCl) is now at 88% in the UK (electronic supplementary material, §4), while estimated global variation is shown in figure 3. In many areas of the world, the gaseous alkaline fraction is over 60% (including NOx) or 80% (excluding NOx). The net result of these changes is that NH4+is now making an increasing relative contribution to the composition of airborne particulate matter, relevant for effects on human health [45]. In parallel, the increasingly alkaline, NH3-rich atmosphere is having substantial consequences for the natural environment, as examined in detail below for lichens and other sensitive plants. (a) Response of lichens to atmospheric ammonia While lichens are well known to be sensitive to SO2concentrations, here we emphasize that NH3is now the primary air pollution driver of lichen distributions in many areas of Europe. To understand the dynamics, we first consider a local-scale transect from Scotland [46] that shows how lichens can change in the vicinity of a poultry farm emitting NH3. Lichens on tree trunks of both Scots pine (Pinus sylvestris) and Sitka spruce (Picea sitchensis), and on branches of birch (Betula pubescens), which are all naturally acid-barked trees, were scored according to a standard methodology [47,48]. In this approach, lichen species are categorized as ‘acidophytes’ (e.g. Usnea,Hypogymnia,Pseudevernia,Bryoria), preferring naturally acidic bark, and ‘nitrophytes’ (e.g. Xanthoria,Physcia), favouring higher levels of nitrogen air pollution (electronic supplementary material, §3) [49]. Using this approach, frequency-based lichen indices for acidophytes (LA) and nitrophytes (LN) were calculated (see electronic supplementary material, §5), where the difference (LAN =LA–LN) distinguishes bark dominated by acidophytes (+value) or nitrophytes (−value). Findings from the local transect are summarized in figure 4, showing how acidophyte species were gradually eradicated between mean NH3concentrations of 1 and 12 µg m−3, with acidophytes on twigs being more sensitive to NH3than those on trunks. Acidophytes on both Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 8 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... 1.6 1.4 1.2 1.0 0.8 NAEI SO2 emissions relative to 1970annual mean (nmol m–3)precipitation pH NAEI NH3 NAEI NOx LTLS SO2 LTLS NH3 LTLS NOx 0.6 0.4 0.2 0 202020102000199019801970196019501940 2015201020052000199519901985 2015201020052000199519901985 160 140 120 100 NH3 HNO3 SO2 SO2(a) NH4 + 80 60 40 20 0 5.50 5.25 5.00 4.75 4.50 (a) (b) (c) Figure 2. (a) Emissions of SO2,NO xand NH3from the UK relative to 1970, comparing the Defra National Atmospheric Emissions Inventory (NAEI) including estimates from the Long-Term Large-Scale (LTLS) model for earlier years [36]. (b) Annual mean concentrations of gaseous NH3,SO 2and HNO3and of aerosol NH4+(for 12 sites), from the UK monitoring network (for further details and error analysis, see Tang et al. [37,38], compared with the earlier trend for five sites (SO2(a)), normalized to the UK mean for 1999–2001. (c) Volume-weighted mean pH of precipitation across the UK based on spatial interpolation of measured values. twigs and trunks were already significantly reduced at the third cleanest location (approximately 1.7 µg m−3, two-sample t-test, two-tail assuming unequal variance, trunks: p<0.001; twigs: p<0.01), where the first nitrophytes on twigs were also recorded. Highest nitrophyte occurrence was recorded at 30 µg m−3, with a significant reduction at 70 µg m−3for both trunks (p<0.001) and twigs (p=0.01). Figure 4dshows that there was also a significant relationship between LAN and measured bark pH. This effect can be largely explained by NH3increasing bark pH nearer the farm (see electronic supplementary material, §5). It is notable that there is no significant difference in the relationship between LAN and bark pH for twigs versus trunks (figure 4d). This indicates Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 9 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... (a)nh3/(nh3+2*so2+hno3+no+no2) all in ppb nh3/(nh3+2*so2+hno3) all in ppb (b) 0.02 150° W 60° S 60° N 30° N 0 30° S 60° S 60° N 30° N 0 30° S 150° E120° W 120° E90° W 90° E60° W 60° E30° W 30° E0 0.04 0.10 0.12 0.14 0.25 0.35 0.45 0.6 0.8 1.0 Figure 3. Global distribution of the gaseous alkaline fraction for 2010 as estimated by the EMEP-WRF global model [44], here calculated based on surface atmosphere mixing ratios (ppbv/ppbv) as NH3/(NH 3+HNO3+2SO2+NOx): (a) including NOx,(b) excluding NOx, since it is unclear to what extent NOxconcentrations influence leaf surface acidity (see electronic supplementary material, §4). that the greater sensitivity of acidophyte lichens on twigs is consistent with the differences in bark chemistry between twigs and trunks. One of the advantages of the local study shown in figure 4 is that it covers a wide range of pollution levels from 0.3 to 70 µg m−3demonstrating its wide relevance for different pollution conditions. The lichen methodology was subsequently applied at 30 sites across the UK [50]. It must be recognized that different tree species also have naturally different bark pH, and therefore the analysis distinguished lichen communities on naturally acid-barked oak (Quercus robor,Q. petraea, recorded where available) from communities on other tree species. LAN was generally not found to be correlated with SO2concentrations (except for a weak relationship for oak trunks, p=0.04, n=11), with a lack of relationship with SO2also found in a later survey [51]. At the UK-scale, trunks and twigs both show reducing LAN score with higher NH3and with higher bark pH, demonstrating the broad relevance of these relationships (figure 5). Substantial Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 16 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... NH3 in air NH3 deposited to bark and thallus NH4 + on thallus NH3 on thallus unspecified toxic effect of NH3 + + + pH effect on ratio NH4 +/NH3 –+ – bark pH bark age (twig versus trunk) +/– tree species Lichen health – + Symplast pH disturbance – plant control of cell uptake + diffusion across cell membranes + Thallus apoplast pH +– unspecified effect of thallus pH Figure 10. Possible mechanisms by which atmospheric NH3pollution affects epiphytic lichens, including both positive (+) and negative (−) effects. Solid lines indicate observed relationships or those directly implied by physico-chemistry. Dashed lined indicate hypothesized relationships. The toxic and pH effects apply especially to acidophyte lichens, but may also apply to nitrophyte lichens at high levels of NH3exposure (figure 4). lichens, adapted to NH4+nutrition (with low NR activity expected), would be more vulnerable to atmospheric NH3. Effects of NH3on lichen pH are also seen at Whim Bog. Electronic supplementary material, figure S8 shows that NH3increased the pH of transplanted Cladonia portentosa thalli, confirming the thallus pH effect (figure 10), with responses seen within one month of transplantation. By contrast, the surface pH of live Sphagnum capillifolium growing in-situ remained unaffected, which may reflect a greater water-holding and buffering capacity of Sphagnum. The importance of such pH effects may also explain the rapid recovery of Cladonia portentosa and Sphagnum spp. following reduction in NH3levels at Moninea Bog. Even though the peat might still contain high N levels, reduced alkalinity from less NH3would be expected to allow rather rapid re-adjustment of surfaces, allowing colonization of acidophyte species. While uncertainties remain over the exact mechanisms, the higher sensitivity to NH3 compared with wet deposited NH4+observed at Whim Bog tends to support this picture. Based on the values of ED50 (with NH3being three times more damaging than NH4+), this suggests that ¾ of the NH3effect on peatland vegetation could be related to pH effects, while ¼ of the NH3 effect is attributable to the common effect of increased nutrient N supply. One of the implications of our findings is therefore to pay more attention to the ‘critical level’ for NH3concentrations for which the UNECE has adopted a value of 1 µg m−3for lichens, bryophytes and associated habitats [65,66]. The extent to which such relationships can be generalized between species, habitats and world regions remains an important question for further work. Each species responds individually according to its nitrogen and pH preferences, sensitivity to NH3toxicity and ability to compete with other species for light and other resources. For example, investigations on Cladonia portentosa from Whim Bog showed that different N forms affect different metabolic pathways [67,68], which may have varying importance between species. It is also possible to identify useful functional groups, as illustrated by the nitrophyte/acidophyte lichen groupings. Calluna vulgaris offers another illustration as this is found to be more sensitive to NH3at Whim Bog than CrossLeaved Heath (Erica tetralix)[56]. If it could be shown (according to [64]) that this reflects a lower apoplastic buffering capacity of Calluna than Erica, then this would encourage further use of buffering capacity as a predictive indicator. In the same way, species/group differences in characteristic lichen acids may also point towards predictive capability with global relevance, which may be tested by the GCRF South Asian Nitrogen Hub. Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 17 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... (b) The future of alkaline air and nitrogen policy The higher sensitivity of vegetation to gaseous NH3compared with wet deposited NH4+and NO3−has direct implications for the success of past SO2and NOxemission reductions in protecting ecosystems. While the acid rain problem has now been addressed in the UK and most of Europe, the modest reductions in NH3emissions mean that alkaline air is emerging as a new ecological challenge. The data presented here focus on naturally acidophyte species, which appear to be especially vulnerable to alkaline air. It remains to be tested whether naturally basic habitats, such as chalk grasslands, would be less vulnerable to ammonia. Already there are indications that NH3concentrations are actually increasing in some parts of Europe rather than decreasing. While this is partly related to reduced SO2and NOx concentrations leading to increased NH3lifetimes, as reflected in NH3monitoring for remote areas [38], there is also concern about climate change impacts on NH3concentrations. As most NH3globally results from volatilization processes, climate warming will increase NH3emissions [69,70]. Strategies to address alkaline air therefore need to include measures that both reduce NH3emissions directly [71] and minimize climate change drivers. In addition to control of CO2 and CH4emissions, decreasing losses of all N compounds (including N2O, NO and N2to air, and NO3−losses to water) becomes critical to increasing economy-wide nitrogen use efficiency, with multiple benefits for climate, air quality, water quality, biodiversity and stratospheric ozone protection [54,72]. Such a perspective could help transform current efforts to meet the EU National Emission Ceilings commitments for 2030, as well as many other policy goals. This takes us closer to developing the big idea whereby ammonia becomes a key focus in an emerging international strategy to manage the global nitrogen cycle. This is why the historical perspective of §2 is so important, in raising awareness about ammonia. One of the lessons of history is that ammonia has always been of significant societal importance. From its role as part of the alchemists’ objective to prepare Gold and the Elixir of Life, to its economically high value as a luxury product of international trade, ammonia continues today to be important in sustaining humanity through nitrogen fertilizers and biological nitrogen fixation. If society is to learn to manage nitrogen better, then these stories can help by raising wider awareness. Ultimately, it may be the economic value of nitrogen that counts most. It has been estimated that global N losses to the environment amount to around 200 million tonnes [73,74]. This means that at a nominal market price of US$1 per kg N, a goal to ‘halve nitrogen waste’ from all sources by 2030 would offer a circular economy opportunity worth US$100 billion per year, amounting to an annual saving of approximately 12 kg N per person (cf. §2a). These issues have recently been recognized in the first Resolution on Sustainable Nitrogen Management adopted at the UN Environment Assembly (UNEP/EA.4/Res.14), with the ambition to halve nitrogen waste adopted in the Colombo Declaration [75]. The follow-up to these activities is bringing ammonia and air pollution together as part of the global nitrogen challenge, by working to establish an Interconvention Nitrogen Coordination Mechanism (INCOM), with targeted science support through the International Nitrogen Management System (INMS) [54,72]. Together these activities can be expected to emphasize how ammonia and the wider nitrogen cycle must be at the heart of the solutions needed for both environment and economy in working towards the UN Sustainable Development Goals. Data accessibility. Data associated with this paper are included in the electronic supplementary material. Authors’ contributions. The article was conceived and written by M.A.S. with text contributions from N.v.D., M.R.J., L.J.S., D.F., M.I.N., S.M. and P.A.W. The air quality measurements were made by Y.S.T., A.S., S.L., I.D.L. and N.v.D. and coordinated by C.F.B. with input from M.A.S. and D.F. Emission data were prepared by U.D., while M.V. performed the global analysis of gaseous alkaline fraction. Measurements at Whim Bog were made by M.R.J., N.v.D., S.L., I.D.L., L.J.S., M.I.N., S.M., with data analysis and interpretation by P.E.L., N.v.D., L.J.S., S.M. and M.A.S. The South Asian element is contributed by M.V., S.C., C.J.E., M.J., M.I.N., A.M., C.E.S., M.A.S. and other authors. The lichen surveys were coordinated by M.A.S., I.D.L., N.v.D. and P.A.W.; the analysis at Moninea Bog was led by M.A.S., I.D.L., N.v.D. and P.C., with input from S.M. and Y.S.T. The historical perspective was prepared by M.A.S. and the policy/future perspective prepared with input from M.A.S., C.M.H. and D.F. Downloaded from https://royalsocietypublishing.org/ on 26 September 2021 18 royalsocietypublishing.org/journal/rsta Phil.Trans.R.Soc.A378: 20190315 ............................................................... Competing interests. We declare we have no competing interests. Funding. This study supported by the UK Natural Environment Research Council (NERC, including grant no. NE/R016429/1 and NE/R000131/1 as part of the UK-SCAPE and SUNRISE programmes delivering National Capability), the Department for Environment Food and Rural Affairs, the Northern Ireland Environment Agency (NIEA), the UK Joint Nature Conservation Committee, the NEWS India-UK Virtual Joint Centre on Agricultural Nitrogen (supported through the Newton-Bhabha Fund, by the UKRI and the Indian Department of Biotechnology), the UKRI Global Challenges Research Fund (South Asian Nitrogen Hub), the EU NitroPortugal project and the ‘Towards INMS’ project of the Global Environment Facility (GEF) and UNEP. Acknowledgements. We gratefully acknowledge funding from the UK Natural Environment Research Council (NERC, including NE/R016429/1 and NE/R000131/1 as part of the UK-SCAPE and SUNRISE programmes delivering National Capability), the Department for Environment Food and Rural Affairs, the Northern Ireland Environment Agency (NIEA), the UK Joint Nature Conservation Committee, the NEWS India-UK Virtual Joint Centre on Agricultural Nitrogen (supported through the Newton-Bhabha Fund, by the UKRI and the Indian Department of Biotechnology), the UKRI Global Challenges Research Fund (South Asian Nitrogen Hub), the EU NitroPortugal project and the ‘Towards INMS’ project of the Global Environment Facility (GEF) and UNEP. We thank Kate Mason for literature support, Geertje Fischer for translations from Karimov (1957), Tony Simcock of the History of Science Museum, Oxford, and UK site operators, including those listed in electronic supplementary material, table S6. References 1. 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