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scientific Nitrogen cycle and world food production Vaclav Smil Distinguished Professor in the Faculty of Environment, University of Manitoba, Winnipeg, CANADA. http://www.vaclavsmil.com

Summary

PIn the biosphere nitrogen has the most complex cycle of all circulating elements. Its incessant reuse makes life on Earth possible. Traditional agricultures supplied limited amounts of the nutrient by recycling organic wastes and by planting leguminous crops. Only the Haber-Bosch synthesis of ammonia, first commercialised in 1913, removed this key constraint on crop productivity. Global agriculture has become steadily more dependent on synthetic nitrogenous compounds without whose applications we would not be able to produce roughly half of today’s world food. This high, and rising, dependence exacts a considerable environmental price, as the losses of nitrogen fertilisers lead to contamination of waters, eutrophication, and excessive atmospheric deposition and emissions of a potent greenhouse gas. Inefficient use of nitrogenous fertilisers is also an obvious economic loss and a waste of natural gas, the prime feedstock and energiser of ammonia synthesis. There is no single measure that could substantially cut these losses but they can be reduced by careful agronomic management and (most effectively, but controversially) by moderate consumption of animal foodstuffs. In any case, more nitrogen will be needed to feed the additional 1.5-2 billion people that will be added to the global population before its growth levels off later in this century.

Glossary and phosphorus (P) which results in activity. excessive plant (principally algae) Eutrophication: degradation of Troposphere: lowest layer of the growth and decay. water quality owing to enrichment earth’s atmosphere, below the by nutrients, primarily nitrogen (N) Anthropogenic: produced by human stratosphere.

9 12 6 Abbreviations Gt, gigatonne, or 10 tonnes, 10 kg. Mt, megatonne, or 10 tonnes. Introduction constituent of all living matter structural compounds. The three Life on Earth would be (typically 45-50% of dry cycles are remarkable because of impossible without incessant weight). Proteins cannot be their complexity, the cycling of key elements that made without nitrogen, and importance of microbes in their make up biomass. Three cycles – disulphide bridges make the functioning and because the those of carbon, nitrogen and proteins three-dimensional, cycled elements are transported sulphur – are particularly ready to enter into myriads of by both air and water and hence noteworthy: carbon is, of enzymatic reactions. Proteins able to move far away from course, the dominant also act as signalling and their sources. Relative neglect and many references to papers published (about 150 Mt N) as is formed by in scientific journals whose content will natural processes (biofixation, existential necessity never become widespread public lightning). There is no possibility that oncerns about rapid global knowledge. we will be able to produce food warming – anthropogenic without nitrogen. Therefore, the Cemissions of carbon dioxide This attention disparity is curious nitrogen cycle and human interference (CO2) and the resulting planet-wide because human interference in the in its functioning should get at least as rise of tropospheric temperatures and nitrogen cycle is incomparably more much attention as our current (and I massive than our perturbance of the alteration of carbon cycle – have come would argue exaggerated) carbon cycle. This is because most of to dominate not only media attention preoccupation with global climate the disruption is due to that most but also scientific debates in general change. fundamental of all energy conversions, and environmental concerns in the production of food. In absolute particular. A simple search of Google terms anthropogenic emissions of Understanding the cycle News reveals the information gap. In carbon from fossil fuel combustion Studies of the nitrogen cycle go back January 2011 the site listed more than (nearly 9 Gt C/year) are less than 10% to the period of pioneering research 700 items for the carbon cycle but of the annual carbon uptake by that laid the foundation of modern life fewer than 90 items for the nitrogen terrestrial photosynthesis. In contrast, sciences during the 19th century (Smil cycle. I would argue that the real human activities (fertilisers, planting of 2001). , one of the public awareness gap is much greater legumes and emissions of nitrogen founders of organic , than this, an order of magnitude oxides from combustion) now release formulated the law of the minimum difference, as the comparison includes about as much reactive nitrogen (plant growth is limited by the WORLD AGRICULTURE 9 10 6/4/11 12:20 Page 1

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‘With average crop yields remaining at the 1900 level the crop harvest in the year 2000 would have required nearly four times more land and the cultivated area would have claimed nearly half of all ice-free continents’

element that is present in the soil in inherently low, typically less than 0.5% America. Eventually China, the world’s the least adequate amount), published in cereal straws, 2-4% in animal most populous country, became, and the first concepts of global biospheric manures, and nitrogen losses before remains, the largest user as well as the cycles and recognised the importance and after their application are high. largest producer of synthetic nitrogen of nitrogen in crop production by These facts necessitate massive labour- (FAO 2011). contrasting it with forestry: Agriculture intensive applications of farmyard differs essentially from the cultivation manures in amounts commonly in The role of synthetic nitrogenous of forests, inasmuch as its principal excess of 10 t/ha. Bird guano has a fertilisers – initially a variety of object consists in the production of higher N content but its resources compounds, most recently dominated nitrogen under any form capable of were limited. Chilean nitrates contain by urea – is perhaps best illustrated by assimilation; whilst the object of forest about 15% N but their exports could comparing typical grain yields in 1900 culture is confined to the production satisfy only a small share of the with the year 2000. In 1900 traditional of carbon (Liebig 1840). potential global demand. Moreover, cultivars received virtually no synthetic the first synthetic products, nitrogen fertilisers, whereas in the year Jean-Baptiste Boussingault (1802- ammonium sulphate from coking and 2000 high-yielding cultivars were 1887) found that the nutritional value grown with an adequate nitrogen synthetic cyanamide (CaCN2) were of fertilisers is proportional to their also available only in limited quantities supply (Smil 2011). This, together nitrogen content and demonstrated and were rather expensive. with advances in breeding (producing that legumes can restore nitrogen to short-stalked cultivars with high the soil. (1814- harvest indices) and chemical 1900) and Joseph Henry Gilbert Synthetic fertilisers and protection (herbicides and pesticides) (1817-1901) initiated the first food production has more than tripled the average US continuous experiments with crops wheat yields during the 20th century All this changed with unexpected receiving different amounts of and the analogical multiples are 5.8 rapidity just before the outbreak of fertilisers and demonstrated, beyond for France and 3.8 for China. in the World War I. In early July 1909, after any doubt, that nitrogen fertilisers USA average yield of corn, the years of intensive experiments, Fritz (followed by phosphates) are the key country’s most important field crop, Haber (1868-1934) succeeded in to higher grain crop yields. In 1877 rose more than five-fold during the synthesising ammonia from its Théophile Schloesing (1824-1919) 20th century, from 1.6 t/ha to 8.5 elements with the help of an iron- proved the bacterial origins of t/ha. Japan’s average rice yield, already based catalyst (Smil 2001; nitrification, in 1885 Ulysse Gayon relatively high in 1900 (2.2 t/ha), Stoltzenberg 2004). Within four years (1845-1929) and his assistants closed increased nearly three times before of this laboratory bench the cycle by finding denitrifying reaching a plateau between 5.8-6.5 bacteria that can reduce nitrates and, demonstration, BASF, Germany’s t/ha during the 1980s. Nationwide largest chemical company, had a via NO and N2O, return N2 to the yield maxima for rice are 6-8 t/ha, in atmosphere. In 1886 Hermann commercial process ready: Carl Bosch East Asia and California. Hellriegel (1831-1895) and Hermann (1874-1940) was the engineer Wilfarth (1853-1904) solved the responsible for this remarkable With average crop yields remaining mystery of leguminous nodules as the achievement. Haber-Bosch synthesis of at the 1900 level the crop harvest in sites where biofixation (conversion of ammonia made it possible to mass- the year 2000 would have required produce inexpensive nitrogenous atmospheric N2 into NH3) takes place. nearly four times more land and the fertilisers but their use remained cultivated area would have claimed The nitrogen cycle (Fig 1) and its key limited during the inter-war years. nearly half of all ice-free continents, role in agricultural productivity were Ammonia synthesis took off only after rather than under 15% of the total thus well understood by the end of World War II, its global output rising land area that is required today (Smil the 19th century and this very from 3.7 Mt N in 1950 to 85 Mt N by 2011). A different perspective has knowledge led to growing concerns the year 2000 and to about 133 Mt in been quantified by Burney, Davis and about future harvests: where will the 2010, with about 75% of the total Lobell (2010): they calculated that countries with growing populations used as fertiliser (Table 1). European, between 1961 and 2005 increased and with rising demand for better North American and Japanese crop yields had a net effect of nutrition get the additional nitrogen agricultures were the first beneficiaries avoiding emissions of up to 161 Gt C. needed to sustain higher crop yields? of inexpensive nitrogenous fertilisers. At the same time, these high levels of None of the options available during By the 1960s rising nitrogen production have made modern the 1890s could solve the challenge. application made it possible to realise cropping highly dependent on Traditional recycling of organic wastes high yields of new short-stalked wheat constant inputs of nitrogen (Table 1) could supply only a limited amount: and rice cultivars planted in low- supplemented by phosphorus, the nitrogen content of these wastes is income countries of Asia and Latin potassium and micronutrients. 10 WORLD AGRICULTURE 11 6/4/11 12:22 Page 1

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Fig 1 Nitrogen cycling in the global agroecosystem. Stores are shown as rectangles and flows as valves. The cycle is subdi- vided into its three principal environmental compartments (atmosphere, soils and waters) and all flows affected or domi- nated by human actions (and hence the targets of possible efficiency improvements) are shown in red while the flows mediated or dominated by bacterial metabolism are in blue. The latest available crop production, livestock and statistics from FAO and IFA and nitrogen contents from Smil (2001) were used to calculate the stores and flows as annual averages for the period 2005-2009. Their accuracy varies from high (, food) to poor (runoff, denitrification). Food (30 Mt N) corresponds to average global per capita daily intakes of 50 g of plant and 25 g of animal protein (excluding aquatic species). The difference between fixation and fertilizers is ammonia used as feedstock in chemical syntheses. WORLD AGRICULTURE 11 12 8/4/11 13:16 Page 1

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Plate 1: Rice fields in terraced hills of South China's Yunnan province: Asia's rice cultivation benefits from high nitrogen applications but it has generally low nitrogen use efficiency, often less than 30%, due to high leaching and denitrification losses. Photograph: Jialiang Gao

Synthetic nitrogenous fertilisers now maximum yields led to steadily higher still higher: even with optimised provide just over half of the nutrient applications of nitrogenous applications they can exceed 70% and received by the world’s crops; the rest compounds, now commonly with traditional applications they can comes mostly from natural and exceeding 100 kg N/ha for the most be more than 80% (Fan et al. 2007). managed (leguminous crops) productive wheat, rice and corn crops. biofixation, organic recycling Two main factors have changed that Consequences of these losses have (manures and crop residues) and trend: (1) higher prices, reflecting the been well documented (Sutton et al. atmospheric deposition. Without the higher cost of natural gas (after World 2011): leaching of nitrates into use of nitrogen fertilisers we could not War II methane (CH4) largely ground water, rivers, ponds and lakes; secure enough food for the prevailing displaced coal hydrogenation as the expanding dead zones in coastal diets of nearly 45% of the world’s main source of hydrogen and it also ocean waters, resulting from recurrent population, or roughly three billion became the principal energiser of the eutrophication; atmospheric people. These diets are excessive in Haber-Bosch process) and (2) deposition of nitrates and ammonia rich countries, adequate in China, but concerns about intensifying environ- affecting natural ecosystems; higher inadequate in much of Africa. The mental impacts. Inherent complexity emissions of nitrous oxide (N2O), now reason for this is that about 85% of all of the nitrogen cycle and the ubiqui- the third most important greenhouse food protein comes from cropping, tous roles of bacteria in its functioning gas following CO2 and CH4. The whereas only 15 % is derived from present many routes for undesirable global extent of these losses is bound grazing and aquatic catches. In China losses from an agroecosystem to increase because at least three synthetic fertilisers already account for receiving high nitrogen applications billion people need substantially better more than 60% of all nitrogen inputs (Bothe, Ferguson and Newton 2007). diets and hence higher nitrogen (Ma et al. 2010) as they do in India applications to their food crops. The (Pathak et al. 2010). By 2025 more Volatilisation, leaching, soil erosion need is most obvious in sub-Saharan than half of the world’s food and denitrification usually claim most Africa where typical fertiliser production will depend on Haber- of the applied nutrient. Although grain application rates are an order of Bosch synthesis, and this share will crops can recover as much as 85-90% magnitude below the recommended keep rising for at least several more in small-scale experiments using 15N- levels (Goulding, Jarvis and Whitmore decades. Unfortunately, this will cause labelled fertiliser (Krupnik et al. 2004), 2008). Of course, our dependence on even greater nitrogen losses in the actual field recoveries are rarely above synthetic nitrogenous fertilisers could environment. 50%. Nitrogen use efficiencies in be cut if we chose to reduce our major EU agricultures range from just intakes of animal foodstuffs – but it 38% in France and the Netherlands to will grow, as dietary transitions change Inefficient fertilisation and 42% in Germany and 44% in Italy the pattern of typical food its environmental impacts (Oenema et al. 2009). In China’s consumption in the opposite Low fertiliser prices and the quest for paddy fields (Plate I) typical losses are direction. 12 WORLD AGRICULTURE 13 8/4/11 13:17 Page 1

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Dietary transitions and demand for nitrogen Rising incomes, urbanisation and industrialisation, the higher participation of women in the labour force and decreasing size of families, has led to a universal transformation of traditional diets. These diets, dominated by a few staple cereals, legumes and tubers, are changing to diets with much lower shares of all staple foods, but with a higher consumption and greater variety of vegetables and fruits and, above all, with much higher intakes of meat, dairy products, eggs and aquatic species. While the speed of this transition has been highly country Table 1: World production of synthetic nitrogenous fertilisers, 1900-2010 (all specific the eventual outcome always values are in Mt N/year rounded to the nearest 100,000 t) results in a much higher demand for nitrogen. Very few countries can secure most of the additional protein demand by grazing or by increased fish catch and the only option is a average efficiency of fertiliser uptake lower average incomes, this is not a much expanded cultivation of feed by plants remains below what should popular course to follow. This leaves us crops, now globally dominated by be achievable by good agronomic with better agronomic management, a corn and soybeans, or their import. practices. My calculations show the portfolio that includes split Inherent inefficiencies of animal overall nitrogen efficiency of the applications and balanced use of metabolism mean that the countries global food system to be no more fertilisers, precision farming, optimised with a high per capita meat supply than 15%, the US rate is no better crop rotations, low-protein animal have the diets with the highest than about 12% (Howarth et al. 2002) feeding and the use of expensive slow- nitrogen cost (that is the lowest overall and Ma et al. (2010) calculated the release compounds: some of these nitrogen use efficiency). Spain is now ratio for China’s food supply to be measures have already helped to lower the European leader with an annual only about 9%. nitrogen losses in the EU (Oenema et supply of about 110 kg of Obviously, even relatively small al. 2009), US and Japan – but much meat/capita, while the US supply reductions in the average meat more will have to be done in order to averages more than 120 kg/capita. consumption would have notable reconcile future needs for more Moreover, the nitrogen cost is effects on overall nitrogen losses. But nitrogen with the quest for high excessive in those countries where in the absence of higher meat costs, or environmental quality.

Howarth, R.W., Boyer, E.W., Pabich, Ecosystems and Environment 133, 280-288. References W.J. and Galloway, J.N. (2002). Nitrogen Pathak, H., Mohanty, S., Jain, N. and Bothe, H., Ferguson, S.J. and Newton, use in the United States from 1961-2000 W.E. Biology of the nitrogen cycle. and potential future trends. Ambio 31, Bhatia, A. (2010). Nitrogen, phosphorus, Amsterdam, Elsevier, 2007. ISBN 88-96. and potassium in Indian agriculture. Nutrient Cycling in Agroecosystems 86, 9780444528575 Krupnik, T. J., Six, J., Ladha, J. K., 287-299. Burney, J., Davis, S.J. and Lobell, D.B. Paine, M. J. and van Kessel, C. (2004). (2010). Greenhouse gas mitigation by An assessment of fertilizer nitrogen Smil, V. Enriching the Earth: Fritz agricultural intensification. Proceedings recovery efficiency by grain crops. In: Haber, Carl Bosch, and the of the National Academy of Sciences 107, Agriculture and the nitrogen cycle. transformation of world food 12052-12057. Assessing the impacts of fertilizer use production. Cambridge, MA, The MIT on food production and the Press, 2001. ISBN 0-262-19449-X Fan, M, Fan, Shihua ,L., Rongfeng, J., environment (A. R. Mosier, J. K. Syers Xuejun L., Xiangzhong, Z., Keith, W., and J. R. Freney, eds). SCOPE 65, Smil, V. Harvesting the biosphere: Goulding, T. and Fusuo, Z. (2007). 193–207. Washington, DC, Island Press. How much we have taken from nature. Nitrogen input, 15N balance and Liebig, J. von. Chemistry in its Cambridge, MA, The MIT Press, 2011. In mineral N dynamics in a rice–wheat applications to agriculture and press. rotation in southwest China. Nutrient physiology, p.85. London, Taylor & Cycling in Agroecosystems 79, 255–265. Stoltzenberg, D. Fritz Haber: Chemist, Walton (1840). Nobel laureate, Jew. Philadelphia, FAO (Food and Agricultural Ma, L., Ma, W.Q., Velthof, G.I., Wang, Chemical Heritage Press, 2004. ISBN 0- Organization) (2011). FAOSTAT: F.H., Qin, W., Zhang, S. and Oenema, O. 941901-24-6 Fertilizers. (2010). Modeling nutrient flows in the http://faostat.fao.org/site/575/default. food chain of China. Journal of Sutton, M.A., Howard, C.M., Erisman, aspx#ancor Environmental Quality, 39, 1279-1289. J.W., Billen, G., Bleeker, A.,Grennfelt, P., van Grinsven, H. and Grizzetti, B., (eds.) Goulding, K., Jarvis, S. and Whitmore, Oenema, O., Witzke, H.P., Klimont, Z., A. (2008). Optimizing nutrient Lesschen, J.P. and Velthof, G.L. (2009). The European Nitrogen Assessment: management for farm systems. Integrated assessment of promising Sources, effects and policy perspectives. Philosophical Transactions of the Royal measures to decrease nitrogen losses in Cambridge, Cambridge University Press, Society B 363, 667-680. agriculture in EU-27. Agriculture, 2011. ISBN: 978110700612

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