GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 13, NO 2, PAGES 647-662, JUNE 1999 Nitrogen in crop production: An accountof global flows Vaclav Smil Departmentof Geography,Universityof Manitoba,Winnipeg,Manitoba,Canada. Abstract. Human activitieshaveroughlydoubledthe amountof reactiveN that entersthe element's biospheric cycle.Cropproduction is by far thesinglelargestcauseof thisanthropogenic alteration. Inorganic fertilizers nowprovide 80TgN yr-1(Tg= 1012g),managed (symbiotic) biofixation addsabout20TgN yr-1, andbetween 28and36TgN yr-1arerecycled in organic wastes.Anthropogenic inputs(includingN in seedsandirrigationwater)now supplyabout85% of 170 (151-186) Tg N reachingthe world'scroplandevery year. About half of this input, 85 TgN yr-1, istakenupbyharvested crops andtheirresidues. Quantification ofN losses fromcrop fields is besetby major uncertainties.Lossesto the atmosphere(denitrificationand volatilization) amount to26-60TgN yr-1, whilewaters receive (fromleaching anderosion) 32-45TgN yr-1 TheseN lossesare the major reasonbehindthe growingconcernsaboutthe enrichmentof the biospherewith reactiveN. The bestevidencesuggests thatin spiteof somesignificantlocal and regionallosses,the world'sagriculturallandaccumulates N. The additionof 3-4 billionpeople beforetheyear2050 will requirefurthersubstantial increases of N inputin cropping,but a large shareof this demandcancomefrom improvedefficiencyof N fertilizeruse. 1. Introduction the nutrient suppliedby biofixation; outputsinclude, besidesthe Human interferencein the global nitrogencycle hasbecomea topic of increasingresearchattention[Smil, 1990, 1991, 1997a; Kinzig and Socolow, 1994; Galloway et al., 1995' Jordan and Weller, 1996; Vitousek et al., 1997]. Compared to the preindustrial era, human activities have roughly doubled the amountof reactive N that entersthe element'sbiosphericcycle [Galloway et al., 1995; Smil, 1997a]. These compoundsinclude NOx (NO andNO2) andotheroxygenated single-Nspecies (the harvested biomass, thelosses dueto gaseous emissions of NO, N2 andN20, volatilization of NH3, leaching, soilerosion,andlosses from tops of plants. In conclusionI evaluate the N balanceof the global cropping and offer a brief assessmentof ways to reduce the existingN burden. Many quantifications in this paper (i.e., nitrogen removed from fields in crops and in crop residues and nitrogen lost in leaching and in eroded soils) are my original calculationsbased on the best available twocategories jointly designated asNOy), NH3 andNH4 +(labeled detailed in NHx), and organicN, and therehasbeenalsoan increasein concentrations of N20, a greenhouse gas. Effectsof this N statistics and on other relevant information the text; others are derived from a wide-ranging surveyof rapidlyincreasing literatureon nitrogencycling. Becauseof our poor understanding of many fluxesof the enrichment range from atmospheric changes (higher complexnitrogen cycleandbecause of considerable spatial,as concentrations of N Ox, NO3-,andNHx) to alterations of terrestrial wellassecular, variationof mostof theflows,quantifications of and aquatic ecosystems (caused by acidification, nutrient leaching,and eutrophication)and to impactson carboncycle. Crop production is by far the single largest cause of human alteration of the global N cycle: Rhizobium bacteria symbiotic with leguminouscropsfix much more N than would be the caseif naturalplant communitieswere occupyingthe samespace,and N global N fluxes shouldavoid an appearance of unwarranted accuracy.Consequently, I will presentall inputsand losses (Tables5 and6) asranges ratherthanassinglevalues. applied to fieldsin synthetic fertilizers (nowabout80Tg N yr-l) Paper number 1999GB900015. The Food and Agriculture Organization's(FAO) worldwide databaseis the most comprehensivesourceof statisticson arable land, annual crop production, and yields (see FAOSTAT Agriculture Data available as http://apps.fao.org,hereinafter referredto asFAOSTAT Data). Accuracyof thesefiguresis high (errorsmostly smallerthan 5%) for high-incomenations,but the FAO must make many in-houseestimatesto fill numerousdata gaps for low-income countries. FAO statisticsalso do not take into account home gardensand backyard plots, which make important nutritional contributions in most Asian, African, and Latin American countries [Hoogerbrugge and Fresco, 1993]. Moreover,someofficial farmlandfiguressubmittedby the FAO's member states are known to be substantial (more than 10%) underestimates.Perhaps the most notable example of such 0886-6236/99/1999GB900015512.00 underestimates is the case of China's farmland: Its real total is is about4 times as large as is the total amountof the elementthat humans fix by burning all fossil fuels [Galloway et al., 1995; Smil, 1997a]. This paper accountsfirst for nitrogentaken up by the global harvest of agricultural crops and their residues, and then it reviewsall major naturaland anthropogenic flows of N reaching, and leaving, the world's crop fields. Quantified inputs include nitrogen in atmospheric deposition, seeds, irrigation water, recycledcrop residues,animal manures,inorganicfertilizers,and Copyright1999by theAmericanGeophyscial Union. 647 2. Global Crop Harvest 648 SMIL: NITROGEN IN CROP PRODUCTION 50% largerthanthe official claim, at least 140 Mha ratherthan95 Mha [State Statistical Bureau, 1997; National Intelligence Council, 1997]. AN ACCOUNT OF GLOBAL FLOWS Table 2. NitrogenIncorporatedin theWorld Crop Harvestof the Mid-1990s Crops HarvestedCrops Crop Residues almost certainly largerthantheFAOtotalof 1.477Gha(1.362 Cereals 30 15 45 Gha of arable land and 115 Mha of land under permanentcrops) and so is the aggregatecrop harvest.Increasesof up to 5% appear to be highly plausible,but the absenceof detailed information neededto quantify and to apportiontheseadditionalamountsof farmland and harvestsprecludesany satisfactorycorrectionsof FAO's statistics even on a continental basis. According to uncorrectedFAO data, the mid-1990s global crop harvest,taken as the mean of 3 years (1994-1996) and excluding the forages Legumes 10 5 15 Sugarcrops 2 I 3 Roots, tubers 2 I 3 Vegetables,fruits Othercrops Forages 2 4 10 I 2 ... 3 6 10 Total 60 Consequently,the actual area of globally cultivated land is 25 Total Harvest 85 All figures arein Tg N yr-l. Freshweights of crops anddryweights grownonfarmland, averaged almost 5.5Pg yr-1in freshweight of cropresiduesfrom Table I aremultipliedby averageN contentsgiven (Table 1). The most accurateway to calculateN takenup by this output is to use N contentsfor harvestedparts (grains, stalks, leaves, by NRC [1972], Watt and Merrill [1975], Smil [1994], and Bath et al. roots,andfruits) of everymajorcrop.I havedonethiscalculation for 40 separatecrops aggregatedinto 8 principal categories. BecauseN contentof cropsis commonlyexpressedin terms of absolutelydry matter,appropriateconversions mustbe donefirst. I used average moisture and N values from National Research Council (NRC) [1972] and Bath et al. [1997]. The mid-1990s [1997]. ground phytomass [DonaldandHatnblin,1976;Gif•brdand Evans,1981;Hay, 1995]. Residualbiomassexpressed as a multipleof harvested yieldscanbe obtained simplyasa ratioof (1-HI)/HI, but this total will be somewhatlargerthan the globalcropharvest of about2.65Pgyr4 of absolutely drymatter commonlyusedresidue/crop(R/C) ratios as the latter indices may not includeplant stubble. contained 50 Tg N yr-l (Table2). Cereals accounted for 60%of Thestandard practice is to quotetheresidue in termsof drytotal dry crop mass,and they also contained60% of all removed N; sugarcropsranked secondin dry mass(16%), but legume cropswere secondin assimilatedN (20%). Calculations of N incorporatedby crop residuescannot be done with a comparableaccuracyas no country keeps statistics on their production.Publishedestimatesof national or global totals of crop residue production were prepared in order to evaluateoptionsfor agronomicmanagementand animal feeding or to find potential contributionsof biomassenergiesor total emissionsof greenhousegases [United States Department of Agriculture (USDA), 1978; Smil, 1985, 1994; Kossila, 1985; Andreae, 1991]. Many figures are available for harvestindices (HI) of major crops, the ratios of crop yield and total above- mattermassand the crop yield at field moisture.The R/C ratios varyamongcultivarsas well asfor the samecultivargrownin differentenvironments. Agronomicfactors(plantingdate, irrigationregime,andN applications) can alsomakesubstantial differences [Priharand Stewart,1991;Robertset al., 1993]. Assumptions concerningaveragestraw/grain(S/G) ratio of cerealswill makea particularlylargedifferencein global calculations. UsingaverageS/Gratioof 1.3,ratherthan1.2,adds almost200 Tg more straw, a total larger than all residual phytomass produced bytheworld'stuberandrootcrops.I triedto minimize sucherrorsbycalculating residue outputseparately for 40 different cropsratherthanjustformajorcropcategories; still, the grand total could not be calculatedwith an error smaller than 5%. Table 1. AnnualGlobalHarvestof CropsandCropResidues in the Mid- 1990s Crops HarvestedCrops CropResidues TotalHarvest Tg of Tg of Tg of Tg of freshweight dryweight dryweight dryweight Cereals 1900 1670 2500 Sugarcrops 1450 450 350 4170 800 Roots, tubers 650 130 200 330 Vegetables 600 60 100 160 Fruits 400 60 100 160 Legumes 200 Oil crops 150 190 110 200 100 390 210 Othercrops Forages 100 2500 80 500 200 280 500 Total 7950 3250 3750 7000 Freshweightsof harvestedcropsare accordingto FAOSTAT Data; dry weightis calculated by usingstandard moisture contents by Wattand Merrill [ 1975]andBathet al. [ 1997];derivationof cropresiduetotalsare described in thetext.All figuresareroundedto avoidthe appearance of unwarrantedprecision. I usedFAO's crop productionfigures,standardvaluesfor water contentof harvestedparts,and fairly conservativeR/C multipliers[Smil, 1994, 1999]. These calculations result in outputs ofbetween 3.5and4.0Pgyr-1ofcropresidues during the mid-1990s; themostlikelytotalof 3.75Pgis about1.4timesthe aggregatecropharvest(Table 1). Cerealstraws,stalks,andleaves accounted for 2/3 of all residual phytomass, andsugarcanetops andleaveswerethe secondlargestcontributor. Justover60% of all residualphytomass were producedin low-incomecountries, andcloseto 45% of it wereoriginated in thetropics.Substantial interspecificand intraspecificvariationsresultin a ratherbroad range of N contentsof cereal straws(0.4-1.3%, valuesaround 0.6%arecommon); onlyleguminous straws arerelatively N-rich. Thetotalremoved in residues amounted to about25 Tg N yr-1 duringthemid-1990s or 1/3of thetotaltakenupbycropbiomass (Table 2). Quantification of annualharvests of foragesgrownon arable land (alfalfa, clovers,vetches,and variouslegume-grass mixtures)canbe doneonlyapproximately. Thesecropsinclude all-legume or legume-grass swards cultivated intermittently on arableland,eitherfordirectforaging or,moreoften,forroughage SMIL: NITROGEN IN CROP PRODUCTION feed (hay and silage), as well as a variety of greenmanures,i.e., leguminousspecieswhich are plowed under after 40-80 days of growth.FAO doesnot keep track of thesecrops,but there is no doubtthat their worldwide extent hasbeendeclining:diffusionof intensivegrain monocultures and wideruseof syntheticfertilizers have been the main reasons for these reductions [Smil, 1993; Wedinand Klopfenstein,1995]. I have consultedstatisticalor agriculturalyearbooksfor about 20 of the world's largest countriesin order to derive the most likely range of the land under forages grown on cropland: between 100-120 Mha in the mid- 1990s, with green manures accounting for no more than 20% of the total area. Fairly conservativeassumptionsabout meandry-matterharvests,5 Mg AN ACCOUNT OF GLOBAL FLOWS 649 furtherdownwind beforetheyareprecipitated ordeposited in dry form. Dry and unpollutedregionshave the lowest ratesof N deposition,while the annualinputsin the mostintensively farmed, industrializedand denselypopulatedareasof North America,EuropeandAsiaarecommonly anorderof magnitude higher(seetheNationalAtmospheric Deposition Program's data available as http://nadp.nrel.colostate.edu/NADP, hereinafter referredto asNADP Data,andErisman[ 1995]). U.S. regionalmeansof N depositedin precipitationare an excellentillustrationof thesedifferences (seeNADP Data).Most of thecountrywestof the Mississippi annuallyreceives just 1-2 kgN ha-1inwetdeposition, withNH4+inputs negligible nearly everywhere west of the Rocky Mountains, while total N in ha-1foralfalfa(planted onabout30%of cropland pastures) and4 precipitation averages over7 kg N ha-1in thecoastal Northeast, Mg ha-i for otherleguminous andmixedlegume-grass forages, andit would bemuch higher if asmuch 75%ofthearea's NOx resultin the total yield of about500 Tg containing10 Tg N. This would increasethe mid-1990s global dry-matter crop harvestto emissions werenot exportedoutto the AtlanticOcean[ Jaworski et al., 1997]. Europehas even greaterregionaldifferences:At about7 Pg yr-1, withabout85 Tg N yr-1incorporated in this over 20kgN ha-1, theannual rates ofNH4+inprecipitation inthe phytomass(Tables 1 and 2). Netherlands, northeastern France,andsouthern Englandaremore than20 timesashighas thosein southern Spainor Italy [Van 3. Nitrogen Inputs Leeuwen et al., 1996]. I used separate estimates ofcontinental averages ofwetNOy A smallpart of harvestedN returnsto fieldsin plantedseeds andNH x deposition rates,derivedfrom long-termdeposition and tubers.All fields receiveN in dry and wet depositionof measurements(see NADP Data and Erisman [1995]), from airbornecompounds andin recycledrootsandstubble.Irrigated emissioninventories[Bouwmanet al., 1997] and from fields receiveadditionalN, largely from nitratesdissolvedin approximate globalbalances[BernerandBerner, 1996],and water. More intensiverecyclingof strawsand stalksis common FAOSTATData's farmland statistics to calculate thetotalinput in manyagroecosystems andin all regions,withmixedfarming of about13(11-15)Tg N yr-l. Aswehavenocomparatively animal manuresproduced' in confinement also recycled. widespread andreliablemeasurements of dry deposition, all Biofixationcontributesrelativelysmallamountsof N in dry generalizations are highly uncertain.Minimum estimatescan be fieldsplantedto nonleguminous crops,butit is a majorsourceof derived byassuming thatdryNHx deposition isequal toatleast the nutrientin leguminous culturesandin rice fields.Although 1/3ofthewetfluxand thatdryNOyisequal toatleast 3/4ofthe many fields, especiallyin Africa, have never receivedany wetinput[Warneck, 1988].Theactual rates, particularly fordry inorganicfertilizer,syntheticN compounds are nowthe single NHx deposition, maybemuchhigher[Sutton etal., 1993]. largestinputof thenutrientin theworld'scropproduction. Theseadjustments wouldresultin totaldeposition of about20 (18-22) Tg N on the world'sagriculturalland. As the total 3.1. Planted Seeds and Tubers Thisis a minorinput,whichis fairly easyto quantify.Many agriculturaldata sourcescarry informationon seedingrates, mostlyin termsof massunits per area, sometimesas sharesof harvestedcrops. Mean seeding rates for more than a dozen terrestrial deposition ofNOyandNHx isnowabout 60TgN yrq [Gallowayet al., 1995;Bernerand Berner, 1996],this would meanthatat least1/3 of all reactiveN deposited on landsettles on the farmlandwhichaccounts only for some11% of ice-free surfaces. Thishigherlevelof enrichment is expected owingto a regionsand nonagricultural principalcropsarelistedin detailedfoodbalancesheets prepared closeproximityof agricultural sources of NO x emissions (particularly in Europe,eastern North by the FAOSTAT Data and multipliedby respectiveplanted andeastAsia)andto a large share ofNOxemissions areastabulatedin the FAOSTAT Data. In turn, theseproducts America, were multiplied by averageN contentsof seedsand tubersused to calculateN incorporatedin the globalcropharvest(Table 2). emanatingfrom agriculturalactivities. This procedureresultedin an annualreturnof about2 Tg N in 3.3. Irrigation Water seeds and tubers. About17%of theworld's cropland (250Mha)wereirrigated in 1995,with nearly2/3 of the globaltotalin Asia(FAOSTAT 3.2. Atmospheric Deposition Data). Irrigation waters always contain some N, and its Higherproductionof nitrates (generatedmainlyby oxidation concentrations arerelatively high(morethan5 mgN kgq) in all of NOx released by combustion of fossilfuels)andvolatilization intensively cultivated regions(wherethe leaching of N from aswell asin of NH 3 (from animal wastes,soils receivingammoniacal fertilizersandanimalwastesarethemainsources) fertilizers,andplanttops)havebeenthe maincausesof steadily densely populated andheavilyindustrialized areas(wherehuman increasing wet and dry deposition of N compoundson wastes andindustrial pollutants arethemaincontributors). agriculturalland.Becauseof thebrief atmospheric residence time of ammonia compounds, largeshares of NHx originating from Annual inputs ofthenutrient inirrigation watermaybehigher than 20kgN haq indouble-cropped rice[Wetselaar etal.,1981 ], ortheymaybebelow5 kgN ha-l inthose predominantly rain-fed agriculturalactivitieseither fall back on the agriculturalland from which they originatedor are depositedcloseto the areasof cropsthat receiveonly somesupplementary irrigation.With theiremissions; incontrast, NOycompounds arecarried much average water applicationsof at least 9000-10,000 m3 haq 650 SMIL: NITROGEN IN CROP PRODUCTION [Shiklomanov, 1993; Postel et al., 1996] and with N AN ACCOUNT OF GLOBAL FLOWS high-income and 40% in low-income countries, would return concentrations mostlybetween 1-2mgN kg-l, theannual global about 12 Tg N yr -1 inputsof the nutrientwouldbe about4 (3-5) Tg N. 3.5. 3.4. Recycling of Crop Residues Recyclingof crop re sidues,directlyby leavingthem after the harvestto decay on field surfacesor by incorporatingthem into soil by ploughing,discing,or chiselling,and indirectlyby using them in mulches and compostsor returning them to fields in animalwastes,hasbeenpracticedvigorouslyby everytraditional agriculture, and it remains an essentialpart of modern field management [Smil, 1999]. Besides the nutrient recycling, protection against water and wind erosion, enhanced water storage capacity of soils, and their enrichmentwith organic matterare otherprincipalbenefits[Barreveld, 1989]. Crop residueshave many competinguses:They have been an importantsourceof householdfuel andbuildingmaterialin many low-income countries;they provide indispensablebeddingand feed for animals, particularly ruminants,of all continents;they offer an excellent substrate for cultivation of mushrooms; and they have been used for making paper and as feedstocksfor extractingorganiccompounds.Unfortunately,a significantshare of crop residues is still burnt in fields, an agronomically undesirablepracticewhich also generatesgreenhouse,and other trace, gases[Andreae, 1991]. No country keeps comprehensivestatisticsof crop residue uses. Fairly reliable information on major usesis available for some affluent countries, but elsewhere we have to rely on fragmentarydata and expert estimates.IntergovernmentalPanel on Climate Changeand Organizationfor EconomicCooperation and Development( IPCC and OECD) [ 1997] estimatedthat about 25% of all residues are burnt in low-income countries and that the correspondingsharein affluent nationsis just 10%. The first rate is almostcertainlytoo conservative,especiallywhen one includes the use of residues for fuel: Widespread energy shortagesin deforested rural areas make the residues the only accessible householdfuel for hundredsof millionsof poorpeasants. Chinese estimatesindicatethat at least3/5 of all cropresiduesareburntby rural households[Smil, 1993; Sinton, 1996]. The estimated mean for residue burning in high-income countriesis also most likely too low, as somefairly reliable data on average burn fractions indicate regionally much higher rates both for field and orchardcrops[Jenkinset al., 1992]. Adding up field and householdcombustion,a more realistic assumption would be that 35% of all residues in low-income countries and 15% of all residuesin affluent nationsare burnt.Burningof about 1 Pg of crop residuescontainingroughly 6 Tg N would release, assuming 80% combustion efficiency, almost 5 Tg N. These emissions wouldnotbemadeuponlyof NOx andNH3:30-40% of the element present in the phytomassis convertedduring flamingcombustion directlyintoN 2 [Kuhlbusch etal., 1991]. Feed and bedding account for anywhere between 20-25% of the remainingtotal in high-incomenationsand for up to 1/3 in low-income countries with large numbersof domesticanimals. Other usesare negligible,particularlywhen comparedto inherent errors in estimating the productionof crop residuesin the first place. Consequently,the highestplausiblerecyclingrates,about 70% in high-income and 60% in low-income countries,would return annually about 16 Tg N to the world's croplands.The lowest plausibleestimates,with averagerecyclingratesof 60% in Animal Manures Manure production,and its N content,dependson breed,sex, age, health, feeding, and water intake of animals [S•nil, 1985]. Freshwasteoutputper headcan be estimatedfairly reliably as a shareof animal's live weight, but large variationsin body mass and feeding, especially the differences between confined and well-fed animals in modern settingsand traditional,free-ranging and poorly fed (and often still also hard-working)breeds,make even national means uncertain. Choosing the best means of N content of manures is even more difficult as various reports list twofold to threefold ranges for dairy, pig, and poultry manures[Misra and Hesse, 1983; Whiteheadand Raistrick, 1993; Choudharyet al., 1996]. Powers et al. [1975] found an even greaterrange (0.6-4.9% N) for beef manures.Using the meanslisted in Table 3 and multiplying them by the FAOSTAT Data animal head counts of the mid-1990s resultsin annual voiding of about75 (70-80) Tg N. This is less than severalother recently publishedestimatesby Mosier et al. [ 1998]; Bouwmanet al. [ 1997] and Nevisonet al. [ 1996]. The main reason for this difference is that I am assuming lower averages of body weights and poorer feeds for cattle, sheep,and goatsin low-income countries(they now have about 75% of the world's bovines and almost 80% of all sheep and goats).Even so, my estimatefor nitrogenin cattlemanuremay be still be too large as some sourcecredit Indian cattle manurewith just 0.7% N on a dry-weight basis[Singhand Balasubramanian, 1980]. Quantifying the amount of N returned to cropland is even more uncertain because of the need for concatenated assumptions.Only animals grazing on cropland pastures, harvestedfields, or cover cropsin tree plantationswill deposit their wastesdirectlyon the farmland:This contributionis only a small shareof all N recycledin manure.Wastesproducedby Table 3. AverageAnnualProduction of AnimalWasteSolidsand TheirTypicalNitrogenContent Animals Waste Solids, N, N Output, kghead-l % kghead-l Producedin Losses, Manure NH3-N Confinement, % % Dairy cattle Modem Traditional 2000 1200 4 3 80 45 60 65 36 36 Modem Traditional Waterbuffalo Horses,mules Pigs 1200 900 900 1200 300 4 3 3 3 3 50 30 30 35 10 35 25 35 50 100 36 36 28 28 36 Sheep,goats Poultry 150 8 3 4 10 100 28 36 Nondairy cattle 5 0.3 Thefollowing average liveweights areassumed: modern dairycattle, 500kg;modem nondairy cattle andhorses, 400kg;traditional dairyand nondairy cattleandwaterbuffaloes, 300kg;pigs,100kg;sheep and goats, 40 kg;andpoultry,1.5kg [MisraandHesse,1983,Smil,1983, Nordstedt,1992,andBouwman etal., 1997]. SMIL: NITROGENIN CROPPRODUCTIONAN ACCOUNTOF GLOBALFLOWS animals grazing on permanentpastureswill be unavailablefor recycling to cropland; only manure producedin confinementon mixed farms and in feeding facilities locatedin farming areascan be economicallydistributedto nearbyfields. Recyclingratesrangefrom only about30% in the USA, where about 40% of all animal wastes are voided in confinement 40% of the nutrient in all animal Table 4. Ranges of Published Biofixation Estimates and the Mean Values Used for CalculatingGlobal Biofixationby Major LeguminousSpecies Crops and about 75% of this output are actually returnedto fields [USDA, 1978], to more than 90% in several small European countries [Rulkensand ten Have, 1994]. Even greaterdifferencesare seen in Asia: Hardly any manureis usedas fertilizer in the continent's interior; a large shareof cattle manurein the Indian subcontinent is gatheredfor fuel, while about 80% of China's pig manureis recycled. Using average shares of manure produced in confinement (Table 3) that are nearly identical to those of Bouwman et al. [1997], I calculated the total amount of N voided annually in stables,barns, sheds, and corrals at 30 (25-35) Tg N or about manures. Even if this manure were to be completely recycled its initial N content would be greatly diminished before these organic wastes could enrich agriculturalsoils:with more than 70% of urine N voidedas urea, there are large lossesdue to rapid hydrolysisof the compound and subsequentvolatilizationof NH 3 during collection,storage, composting,and handlingof wastes[SubbaRao, 1988; Eghball 651 Rangesof Published Rangesof Means Estimates*, Used in Calculations, kgN ha-• kgN ha-I Seedlegumes Beans Broad beans Chickpeas 3-160 45-300 30-40-50 80-100-120 3-141 40-50-60 Lentils 10-192 Peas 10-244 30-40-50 30-40-50 Peanuts 37-206 60-80-100 Soybeans Otherpulses 15-450 7-235 60-80-100 40-60-80 Forages Alfalfa 65-600 150-200-250 Clovers 28-300 130-150-170 Otherforages 9-180 80-100-120 * Data are from LaRue and Patterson [ 1981], Heichel [1987], Giller and Wilson[1991],Peopleset al. [1995],and Smil[1997b] et al., 1997; Bouwman et al., 1997]. These losses,together with denitrification and leaching, are especiallyhigh in traditionalsettingswith prolongedstorageof manuresin the open. Depending on the kind of handling and concentrationsof inorganic forms of N, shortagesof essential micronutrients(particularly Mo, V, and Fe presentin the redox centerof nitrogenase[Eady, 1995]), and low soil pH. storage,mostor nearlyall of NH3-N (up to 50% of initially Dozens of N fixation rates from a number of different voidedN), aswell asappreciable amounts of NO3-N andorganic agroecosystemshave been publishedfor such widely cultivated N, may be lost before the applicationto fields. Assumingthat 90% of manureproducedin confinementis eventuallyrecycledto fields (the restis dumpedor recycledto pastures)andreducingits leguminousfood and feed crops as common beans (Phaseolus vulgaris) and soybeans(Glycine max) as well as for suchleading forage species as alfalfa (Medicago) and various clovers initialN content by average NH3-N losses proposed by Bouwman (Trifolium). Almost all publishedvalues have at least three-fold et al. [1997] and listed in Table 3, ! calculated that recycled ranges and much larger differences are common (Table 4). animal manurescontribute about 18 Tg N (14-22) Tg N. I will Particularly notable are low-fixation rates in common beans in estimate specific post-application NH 3 losses in section 4. Latin America, the crop'sregionof origin [Henson, 1993; Tsai et al., 1993]. For lesscommonleguminousspecies,we havetoo few 3.6. Biofixation reliable figures; our knowledgeof fixation rates is particularly Reduction of atmosphericN2 to NH 3 is performed inadequate as far as tropical legumes, be they used for food, enzymaticallyby at least60 generaof cyanobacteria(blue-green fodder, or as green manure, are concerned [Blair et al., 1990; Peoplesand Herridge, 1990]. algae), 15 genera of symbiotic actinomycetes,and, above all, In order to make the best possible estimate of symbiotic some25 generaof free-livingandsymbioticbacteria.By far, the most important symbionts belong to the genus Rhizobium biofixation, I have usedspecificrangesfor eight differentkinds associatedwith leguminous plants. Nearly a generation ago, of seedlegumeslistedin Table 4 (beans,broadbeans,chickpeas, LaRue and Patterson [1981] noted that there was not a single lentils, peas, peanuts, soybeans, and other pulses) whose cultivated areas were taken from FAOSTAT Data. This resulted in legume crop for which we had valid estimatesof N fixation. Rhizobium fixationof 10Tg N yrq Although many new estimateshave been publishedsince that themostlikelytotalof global time, we are still unableto offer reliable, representativevaluesof (rangeof 8-12Tg N yr-1), whileleguminous cropsremoved15 average annual fixation rates even for the most important Tg N yr-1 (Table2). Thismeans thatthesecropsderived 2/3 of leguminouscultivars.This is not surprisingwhenconsidering the their N from biofixation, an averagesharein excellentagreement with numerous studies of biofixation's contribution to N large natural variability of symbiotic fixation, as well as the errorsinherentin techniquescommonlyusedto measurethe rates requirementsof legumes[Hardarson, 1993; Peopleset al., 1995]. This does not mean that there is no transfer of N from seed of N fixation [ Hardarson and Danso, 1993; Danso et al., 1993]. Fixation rates vary enormously with both abundance and legumes to subsequent nonleguminous crops. This eventual persistence of specificRhizobiumstrainsin soils,with the vigor enrichmentdependson the degreeto which legumescan satisfy their total N needs from the biofixation and on the share of the of host plants and with environmental stresses[Ayanaba and Dart, 1977; Broughton and Puhler, 1986]. Major factors fixed N taken up by the harvestedlegume seeds [Hardarson, reducing,or even inhibiting, N fixation includesoil temperature, 1993; Giller et al., 1994]. The latter sharerangesfrom as little as bothtoolittle andtoo muchmoisture, low soil0 2 levels,high 30% for common beans to more than 80% for soybeans. 652 SMIL: NITROGEN IN CROP PRODUCTION Completerecyclingof beanplantresidueswill thustransfermost of the fixed N for eventual use by subsequentcrops;however, soybeans,althoughthey are much more prolific N fixers than beans,may not be able to provideall of the needednutrients,and the crop will have to claim considerableamountsof soil N [Heichel , 1987]. Estimatingbiofixation by leguminouscover cropsis a much greaterchallenge.As alreadynoted,foragesand greenmanures occupy100-120 Mha of farmland.Averagefixationratesof 200 AN ACCOUNT OF GLOBAL FLOWS 3.7. Inorganic Fertilizers This is the mostaccuratelyknown,andnow alsothe single largest, inputintotheglobal N cycle. Mineral compounds (KNO3 andNaNO3)arestillused,buttheirapplications aredwarfedby the use of syntheticfertilizers.Their productionnow begins invariably withtheHaber-Bosch process of NH3 synthesis first introducedcommercially in 1913 [ United Nations Industrial Development Organization and International Fertilizer Development Center(UNIDO andIFDC), 1998].Duringthemid- kg N ha-1for alfalfaand150kg N ha-1forclovers andvetches 1990sthenominalcapacityof theworld'sammoniaplants,now are well supportedby numerous measurements[Frame and Newbould, 1986; Dovrat, 1993; Meetu et at., 1994], but fixation by legume-grass mixturesis muchmorevariable,rangingfrom a justa fewkilograms to morethan250kg N ha-1 [Heicheland Henjum, 1991; Farnham and George, 1994]; I will assumejust usinglargelyCH4 bothasthefeedstock (H source; N is separated fromthe air) andfuel, wasabout115Tg N yr-l [Foodand AgricultureOrganization(FAO), 1997]. Actual synthesis was about95 Tg N yr-1, of whichalmost80 Tg N yr-•was incorporatedin syntheticfertilizerswith the remainderconsumed 50kgN ha-1. A fairlyconservative totalof N fixationin 100-120 by chemical industries and lost during processingand Mha of croplandforagesand green manures(averaging100 kg N ha-1) isthenabout12TgN yr-I (range of 10-14TgN yr4 ). As thesecropsremoveannuallyonly about10 Tg N, therecan be no doubt that they leave behind large amountsof N for subsequentnonleguminouscrops. The actual total is almost certainly somewhat higher as it includes biofixation by leguminouscropsgrown as soil coversin manytree plantations as well fixation by trees and shrubsused in alley croppingand planted along field boundaries and house gardens for feed, fuelwood, and shade[Blair et at., 1990; Gutteridgeand Shelton, 1994]. Biofixation by non-Rhizobiumdiazotrophsis of lesser importance.Some studiesreport valuesfor biofixation by freeliving bacteria and cyanobacteria in cereal fields in humid environments in excessof 20 kg N ha-1 duringthe growing season[Neyra and Dobereiner, 1977], but typical rates in drier environments aremostlylessthan5 kg N ha-1or nomorethan4 (2-6)TgN yr-1fortheworld's cereal, tuber,andoilcropfields. transportation. Consumption data,global,regional,andnational,arereported annuallyby the FAOSTAT Data as well as by the International Fertilizer Association (see the World Nitrogen Fertilizer Consumption reportavailableashttp://www.fertilizer.org). After a slightdeclineduringtheearly 1990s(to 72.5 Tg N by 1993), globalconsumption roseagainto almost79 Tg N in 1995andto nearly 83 Tg N in 1996. Theseconsumption figuresdo not account for a variety of preapplication losses which are particularly largeforthehighlyvolatile NH4HCO3,stilla major fertilizerin China [Smil, 1993]. In addition,someN fertilizersare usedon permanentpasturesand in forests,and increasing quantitiesare alsoappliedto lawns. Ammonia is either used directly as the most highly concentrated (82% N) andthe cheapest N fertilizer(appliedas gas or in aqueoussolutions)or convertedto urea, the most concentrated solidfertilizer(46% N) nowaccounting for nearly 40% of globalN consumption andgreatlypreferredin Asia,the ricefieldscanfix 20-30kg N ha4 duringthegrowingseason. continentwhichnow usesnearly3/5 of the world'sfertilizerN. When including the contributions by Anabaena azollae, a Variousnitratesor compound fertilizers(combinations withP, K, symbiont ofAzotla pinnata, a small floating fern cultivated in andmicronutrients) are alsoused.About60% of synthetic N In contrast, cyanobacteria(mainly Anabaena andNostoe) in Asia'spaddies, whichcanproduce asmuchas50-90kg N ha-I fertilizers are now consumed in the low- and middle-income during 40-60 days [Meelu et aL, 1994], and when taking into accountthe rate of rice multicropping(mean global ratio of about 1.25), cyanobacterialfixation may have contributedbetween4-6 countries, andthenutrientis indispensable for maintaining the Tg N yr-1in 150Mhaof theworld's paddies. A recentdiscovery recentlyachievedstaplefoodself-sufficiency in theworld'smost populous nations(China,India,andIndonesia). Annual applicationmeansof the mid-1990s were around50 of endophytic diazotrophs (Acetobacter and Herbaspiritlum) kgN ha-1of arable landfortheworld, andtheyranged between living inside sugar cane roots, stems, and leaves explains why 10-100 kgN ha-1 forcontinents (AfricaandEurope being the unfertilized crops maintain high yields even after years of extremes). Nationalapplication meanshideenormous regional consecutivecultivation[Boddeyet at., 1995]. Theseendophytes variations: Forexample, theU.S.meanof about50 kg N ha-l is fix annually at least50 kg N ha-I , maxima maybehigherthan madeupof ratesbelow20 kgN ha-1in NorthDakotawheatfields 150kg N ha-1, resulting in therangeof 1-3Tg N fortheworld's towellover200kgN ha4 in Iowacornfields. Application rates 18 Mha of sugarcane. shouldbe alsoadjusted for variousdegrees of multicropping: As calculated above, the total biofixation in crop fields, plantations,and croplandpastures,a combinationof contributions by Rhizobium-legume symbioses in food,feed,forage,andgreen manure crops; symbiotic Azotta-Anabaena fixation in paddies; free-living cyanobacteriaand bacteriain wet and dry fields; and endophyticbacteria in sugar cane, would have been 33 (25-41) High fertilizationratesin Asia'smonsoonal agricultures, where double-andeventriple-cropping is common,are thenhalvedor cut by 2/3 in order to make propercomparisons with those temperate countries whereonlya singlecropisgrownperyear. Duringthe cominggenerationeverypopulouslow-income country,and particularlyIndia, China,Pakistan,Nigeria,and Tg N yr-1 duringthemid-1990s. Thiswaslessthanhalfthetotal Indonesia,the five nationsthat will accountfor morethan40% of massof N appliedin inorganicN fertilizers,but more than all N recycledin crop residuesand animal manures. theworld'spopulation increase by theyear2020[ UnitedNations Organization(UNO), 1998], will have to increaseits N fertilizer SMIL: NITROGEN IN CROP PRODUCTION AN ACCOUNT OF GLOBAL FLOWS 653 applications. In contrast, European applications have been declining,and they will remain stableor will declinefurther with the removal of excessive farming subsidies and with limits imposed due to environmental concerns (see Jongbloed and Henkens [1996] and European Fertilizer Manufacturers Association's Code of Best Agriculture Practice-Nitrogen availableashttp://www.efma.org;referredto asEFMA data). biomass, we havemuchlessconfidence aboutapportioning this 3.8. Fertilizer Recovery Rates huge N loss amongthe major processes that removeN from agroecosystems to the atmosphere andto bothunderground and Calculated inputs sum up to 151-186 Tg N, with additions climates, 55%forcropsin humidclimates, 65%forlegumes, and 75% for croplandforages,by the FAOSTAT Data areassownto thesecropsresultsin a weighted recovery average of about50%, anexcellent confirmation of thecalculated mean.Whilewemay concludewith a highdegreeof confidencethat 1/2 of all N added annuallyto theworld'scroplands is notincorporated in harvested surface waters. closeto 170Tg N yr-1beingmostlikely(Table5). Dividingthe element removed in crops by the estimatesof total N inputs resultsin averageglobal recovery rates of 46-56% (mean 50%). Theseratesserveas an importantmeansof checkingthe validity of presentedcalculations.Data from numerousN intake studies (mostreliablyfrom thoseusing15N)constrain the rangeof plausible recovery rates (their global mean could not be below 35% or above 65%), and they also help to delimit the most likely rate. Analyses of 30 (mostly temperate zone) agroecosystems showedthat 2/3 of them had N recoveryratesbelow 50%, while the most efficient cropping absorbednearly 70% of applied N 4. Nitrogen Losses Both nitrification and denitrification remove soil N as NO and N20, anddenitrification, the closingarm of the biospheric N cycle,restores N2 to theatmosphere. Volatilization of NH3 is responsiblefor large N lossesfrom both animal manuresand fromall ammoniafertilizers.Leachingof highlysolublenitrates andsoil erosiontransfers oftenlargeamounts of N to ground water, and to streams, lakes and coastal waters where the nutrient cancauseserious eutrophication; erosion canalsoremovea great dealof organicN. Therearealsovarious,andoftenconsiderable, N lossesfrom topsof plantsbeforetheharvest. below150kgN ha-i , uptake efficiencies wereashighas60-65% but with higher N application recovery rates scatteredaround [Frissel and Kolenbrander, 1978]. Where fertilization rates were 50%. An extensiveEuropeansurvey found the following N uptake efficiencies:high-yieldingwheatsin France39-57% (from urea) and 38-70% (from ammonia), in England 52-65%, and in the Netherlands52-62%, but in Portugaljust 27-40%, and in Greece only 18-37% [Jenkinson and Smith, 1989]. In Asian rice, typicallyrecoveryratesare between30-35%; they may be as low as 20% and only rarely do they exceed 40% of the applied nutrient [De Datta, 1995; Cassmanet al., 1996]. North American corn recovers between 40-60% [Reddy and Reddy, 1993], and leguminous crops, particularly forages, incorporate generally more of the available (and largely self-supplied) N, usually anywhere between 50-90% [Peoples and Herridge, 1990]. Recovery ratesof N addedto soilsby atmosphericdepositionand irrigationwater are similar to thoseof inorganicN. Multiplying conservativemeansof N recoveryratesfor major cropcategories,35% for rice andfor rainfedcropsgrownin drier 4.1. NOx andN 20 Emissions Two key flows in the biosphericnitrogen cycle, bacterial nitrification (oxidation of NH4+) anddenitrification (reduction of NO3- or NO2-), arethemainsources of NOx (mostlyNO) and N20 emittedfromsoils.Chemicaldenitrification andotherkinds of bacterial metabolisminvolving oxidation or reductionof N alsoyield trace amountsof the two gases.Nitrificationratesare regulated primarilyby theavailability of NH4+;denitrification is controlledmainly by temperature,precipitation,and soil texture, C availabilityand pH [Bouwmanet al., 1993]. Ratesof fertilization,crop varieties,and tillage practicesare the most important management factors determining the emissions.Water-filledporespace(WFPS) appearsto be the key determinantof the relative fluxes of the two gases:NO fluxes peakwith30-60%WFPS,whiletheN20 flowspeakwhenWFPS is between 80-90% [Veldkamp et al., 1998]. Rates of NO and N20 emissions fromagricultural soilsaresohighlyvariablethat Table 5. Annual N Inputs to the World's CroplandsDuring the annual fluxes (derived mostly from short-termmeasurements) range over several orders of magnitude[ Williams et al., 1992; Mid- 1990s Bouwman, 1996]. Inputs Seeds Atmosphericdeposition Irrigationwater Cropresidues 2 2 2 18 3 12 20 4 14 22 5 16 Shepherdet al. [1991] measuredNO-N emissionsequal to 11% of added N in a fertilized soil in Ontario. Typical NO-N lossesare considerablylower, rangingbetween0.02-5.7% of the nutrientappliedin fertilizers[Harrisonet al., 1995; Veldkampet al., 1998]. Consequently,annual means of NO emissionsfrom agriculturalsoils derived from long-termmeasurements range frommeretraces to nearly10kgN ha-1. Potteretal. [1996]used Minimum Mean Maximum Animal manures 16 18 20 Biofixation 25 33 41 the averagerates of 1.5 kg N/ha as NO in global simulations; Inorganicfertilizers 75 78 80 Davidson andKingerlee [1997]foundthemeanof 3.6kg N ha-1 151 169 186 for temperatefields worldwide; Davidsonet al. [1998] usedthe Total All valuesarein Tg N yr-I. Derivations of individual inputratesis describedin the text. All figuresare roundedto avoidthe appearance of unwarrantedprecision. meanof 8.8 kg N ha-1for thesoilsof thesoutheastern United Statesbut admittedit may be somewhathigh. Given this great uncertainty I will assume a conservative rangeof 0.5-4kgN ha-1, 654 SMIL: NITROGENIN CROPPRODUCTION AN ACCOUNTOF GLOBALFLOWS resulting in annual global releasesof 1-6 Tg NO-N from the information, combined with other data, can be used to narrow world's cultivated down the uncertainty. Most of their ratios fit between 1-20; simplemean is about8; and weightedmean(alter discardinga handful of the most extreme outliers) is about 5. Taking the last soils. Recorded N20 emissions alsorangeoverseveralordersof magnitude.Annual meansfor emissionsfrom soilsthat have not beenrecently fertilizedrangemostlybetween 1-5kgN ha-1, and value as the minimum ratio would, with annual emissions of at theaverage amountof fertilizer-induced N20 emissions increases least2 Tg N20-N, generate nolessthan10Tg N orabout10%of over time, and it ranges mostly between 0.5-2% of initial N applications[Harrison et al., 1995]. Veldkampet al. [1998] recordedrates as high as 6.8% in tropical pastureson soils developedfrom volcanicash,and Shepherdet al. [1991] found conversions equal to 5% of applied fertilizer. Manure all N particularly susceptibleto relatively rapid denitrification (that is N introducedin atmosphericdeposition,irrigation water, animal manures,andinorganicfertilizers). Similar rates have been reportedin relatively rare studiesof total denitrification. Rolston et al. [1978] found total applications canincrease N20 emissions, frombothnitrification denitrific•itionfluxes equal to 11-14% of applied N (inorganic and manure)on croppedsites,and Rydenet al. [ 1979] measured and denitriflcation, several-fold compared to fluxes from soil an average loss of about 15% from a heavily fertilized and receivingsome,or no,inorganicfertilizer[Li et al., 1994]. In their model of global N trace gas emissions,Potter et al. irrigatedfarmland,withaverage N2: N20 ratiosbetween 5.6-7.4. Svenssonet al. [1991] found seasonallossesbetween 2-7% just [1996]usedthe rateof 0.8 kg N/ha asN20 as an averageflux for the appliedinorganicN. Lossesequalto 10-15% of N most from cultivated soils; this would produceannually about 1.2 Tg N. Bouwman [1996] recommended the mean of 1.25% of N susceptibleto denitrification would produce annual fluxes between 11-18 Tg N, and, uncertain as this estimate is, it is fertilizer applications,in addition to 1 kg N20-N/ha of backgroundemissions,to be used for large-scale,order-of- unlikelythat the actualflux wouldbe lowerthanthe meanof this magnitude quantifications; thiswouldtranslate to about2.5 Tg N range.Obviously,muchmoreN2 is eventuallyreturnedfrom of annual emissions. agroecosystemsto the atmosphereby denitrification of N compounds whichwereremovedfrom fieldsby leachingandsoil erosion,and carriedaway in harvestedfeed and food crops. Li et at [1996], using their detailed denitrification- decomposition model,estimated totalN20 emissions from the U.S. croplands at 0.5-0.74Tg N yr-1 or 3-4.6kg N ha-l; extendingthe highestrate to the globalcroplandwouldresultin 4.3. Volatilizationof NH3 emissions of upto 7 Tg N yr4 . | will usetherangeof 1-7Tg N Relativelylargeamounts of NH3-N thatcanbe lostduring for globalN20-N emissions fromagricultural soils.Giventhe daysand weeksfollowing applicationsof ammoniafertilizersand enormous variabilityof NO andN20 fluxesfromagricultural animal manures have been a long-standing concern among soilsand from appliedfertilizers,the rangeemergingfrom these agronomists[Terman, 1979; dayaweera and Mikkelsen, 1991]. Reported sharesof initial N loss are as high as 46% within a week for urea and 80% for animal urine in just 3 days [Hargrove, 4.2. Complete Denitrification 1988]. Dry, calcareous soils, surface applications of shallow Estimatingannual return of N2 producedby complete incorporationof fertilizers, and manuresand high temperatures promotethe lossin rain-fed fields. alenitrification is by far the most elusive task in quantifying Volatilization losses are particularly high when ammonia principalfluxes of the global N cycle. Obviously,the processis governedby the samefactorsas N20 generation, with rates fertilizers are broadcastdirectly onto flooded soils [dayaweera and Mikkelsen, 1991]. Principalfactorspromotingthe processare highly dependent on soil water content (high WFPS) and available soilcarbon. Highconcentrations of soilNO3- inhibitthe shallow waters, their alkaline pH, high temperature and high estimates, 2-13Tg yr-1, isnotexcessive. final conversion stepfrom N20 to N and lower the N2:N20 NH4+-Nconcentration, andhigherwindspeeds. Consequently, ratios [Weier et al., 1993]. Reliable direct measurements of completealenitrificationin farmlandsare rare, and alenitrification fluxes in field or regional N balancesare commonly estimatedas residualvaluesafter accountingfor othermajor N losses. the highest volatilization lossesare in heavily fertilized paddy fields in the tropics; dominanceof urea in rice farming makes matters worse as the pH of noncalcareoussoils is temporarily elevatedafter its application[ Hatgrove, 1988]. As with NO andN20 emissions, theenormous variabilityof fluxes from different soils and under different environmental Volatilization losses of the order of 10% within 1-3 weeks of N applicationsare common,and recordedmaxima are above60% or even70%.Volatilization fromnon-NH3 fertilizers is minimal, highlyquestionable. However,withN 2 emissions beingsomuch and large-scale (national or global) means used to calculate largerthanthecombined NO andN20 flux,thereis muchgreater annual losseshave been as low as 1% [ApSimonet al., 1987] for conditions makes the choice of any typical or average value opportunityfor underestimatingor exaggeratingthe overall flux by relatively small shiftsin assumptions.Galloway et al. [1995] basedtheirestimates of totalglobalalenitrification on N2:N20 ratios between 14-32, but, as explained in the following two paragraphs,the most likely ratios for agricultural soils may be much lower. After 5 days of measurementsin four kinds of benchmark soils,Weieret al. [1993]foundN 2 :N20 ratiosrangingfromas low as 0.2 to as much as 245 and, not surprisingly,concludedthat using an average ratio for estimating total alenitrificationfrom N20 field measurements cannotbe recommended. Still, their the UK and as high as 11% [Bouwmanet al., 1997] for the world. Given the still increasinguse of urea and higher intensity of N applicationsin humid and warm environmentsin generaland in Asia'smonsoonalrice fields in particular,worldwide lossesof 812% (10%) of N applied in inorganicfertilizers would produce annual fluxes of6-10(8)TgNH3-Nyr-1. Tothese losses must be addedvolatilization of animal wastesappliedto cropland. Numerous experimentaland fields studiesshow lossesof at least 10-15% of the initial N content within days or weeks after applicationof animal manures,and with surfaceapplicationsof fresh cattle or pig slurriesthe lossesmay be as much as 60-80% SMIL: NITROGEN IN CROP PRODUCTION ofNH3-Nor some30-40%of totalN [Terman,1979;Hansen and Henriksen, 1989]. This means that in addition to the conservativelyestimatedpreapplicationlosses,there will be furthervolatilization lossesof at least15-20%of N appliedin animalmanures or about2-4 Tg N. This wouldbringthe total lossof thenutrientappliedin inorganic andorganicfertilizersto atleast11(8-14)Tg N orroughlybetween 5-10kgN ha-1 AN ACCOUNT OF GLOBAL FLOWS 655 applyingtypicalannualleachingrates(5-30 kg N ha-1) to the sameregionalset,cameup withabout17 Tg N yr-1. To these totals must be added the leaching lossesfrom animal manures: with no less than 10-20% of applied N they would come to 1-3 Tg N yr-1.Annualgloballeaching lossfromagricultural land would be then about 17 (14-20) Tg N, averagingbetween 10-15 kgN ha4 . Neteffects ofannual deposition-volatilization fluxes ofNH3 overcroplandsarehighlyvariable.Changesbothin directionand magnitudetake placeon daily as well as seasonal basis,and in 4.5. Soil Erosion Recent concernsabout soil erosion and its effects on crop spiteof oftensubstantial NH3deposition somesitesmayactually productivity[Pimentel, 1993; Pimentelet al., 1995; Agassi,1995] show small (<1kgN ha-1yr-1) netNH3emissions [Sutton etal., have not been matchedby reliable information about the actual 1993].Moreimportantly, thereis a sizeable NHqfluxfromtops extentand intensityof the processor, moreaccurately,aboutsoil of maturing plants, and I will accountfor theseemissionsat the end of this surveyof N losses. losses in excess of natural denudation. Global assessment of soil degradation[ Oldeman et al., 1990] estimatedthat about750 Mha of continentalsurfacesare moderatelyto excessivelyaffectedby 4.4. Leaching water erosion and 280 Mha by wind erosion,with deforestation Leaching rates depend on levels of fertilization, compounds and overgrazingbeing major causes;mismanagementof arable used(NH3 leachesverylittle in comparison to readilysoluble land was estimatedto be responsiblefor excessiveerosion on NO3), soil thicknessand permeability,temperature,and some 180 Mha of cropland, but no global quantification of precipitation. The single most important land management excessiveerosionwas attempted. determinant of the intensity of leaching is the presenceand Becauseerosionratesvary widely even within a singlefield, quality of the groundcover [Hill, 1991]. Everything else being any large-scalegeneralizationsare merely order-of-magnitude equal, leaching from bare, fallow, or freshly ploughedsoils is indicators.They alsoignorethe complexityof the process:much much higher than beneath row crops, which, in turn, is of the eroded soil is not lost to food production.Larson et al. considerablyhigher than from soilsunder suchdensecover crops [1983] found that very little or no eroded sediment leaves the as legume-grassmixtureswhoserootscan take up large amounts cultivatedland in areaswith gentle relief without any major of added N. surfaceoutlet,the landscapecommonin the north-centralUnited Relatively abundantinformation on nitrate exportsin streams States;andwhenthe sedimentleavesthe land,mostof it maybe and groundwaters[Cole et al., 1993; Canter, 1997] is of little use depositeddownstreamas colluviumor alluvium [Trimble, 1975]. in assessingN leaching from agricultural land as there is no Consequently, evenif croplandswerethe only sourcesof eroded reliable way to separate the contributions of atmospheric soil, the amount of N exported from the fields could not be deposition, sewage and industrial processes from the flux reliably quantifiedby using the relatively abundantdata on the originating in inorganic fertilizers and animal manures.Because transportof suspendedsedimentto the ocean. of its effects on the quality of surfaceand groundwaters,nitrate Short-termratesof croplanderosionhave been measuredand leachinghasreceiveda greatdeal of researchattention[Addiscott estimatedwith varying degreesof accuracyfor many locales et al., 1991; Hill, 1991; Burt et al., 1993], but, as with many other aroundthe world. Their extremesrangefrom negligiblelossesin N fluxes, leaching rates have been measuredmostly over short rice paddiesto morethan200 metrictons(t) ha-1 on steep tropical slopes and in the world's most erodible soils of China's periodsof time (days to monthsafter fertilizer application)and proratingthesefiguresmay underestimatelong-termthroughputs LoessPlateau[Liu, 1988;HamiltonandLuk, 1993].Averagesoil [Valiela et al., 1997]. erosionestimatesfor largerareasare rarely available.Nationwide Annual leachinglossesrange from negligible amountsin arid U.S. inventories,begunin 1977, are a major exception:Recent and semi-aridfieldsto 20-30 kg N ha-1 in rainytemperate annualmeanswere just above 15 t ha-l , with about60% regions. Maximaof over50kgN ha-I arenotunusual in themost contributedby water erosion,and the preliminaryvalue for 1997 heavily fertilized crop fields of northwesternEuropeand the U.S. is about14t ha-• [Lee,1990](seealsoCropland acreage, soil Midwest. Even higher leachinglosseshave beenreportedin some irrigatedcrops[Diez et al., 1997; Prunty and Greenland., 1997], but lossesin many Asian paddy fields are very low. A surveyof 40 agroecosystemson three continents indicated that with erosion, and installation of conservation buffer strips: Preliminaryestimatesof the 1997NationalResources Inventory available as http://www.nhg.nres.usda.gov/land).The first nationwide approximationfor India indicateslossesof at least 13 applications of lessthan150kg N ha-1 leaching equaled about t ha-• forwatererosion alone[Singh etal., 1992],andregional 10% of fertilizer N, while with additionsof more than 150 kg N estimatesfor China [Zhu, 1997] imply a nationalmeanof about ha-1 about20% of addedN waslost[FrisselandKolenbrander, 30 t ha-1. 1978]. Losses of 15-25% of initial N were also measured with repeatedapplicationsof cattle feedlot manure[ Changand Entz, 1996]. Highest leaching rates, on sandy soils, may remove over 60% of N appliedin manure[Hansenand Djurhuus, 1996]. I prepared two kinds of global estimates.The first one, assigningspecificaverageleachingshares(5-25%) to inorganic N applicationsdisaggregatedby 11 major agriculturalregions, Globalmeanof 20 t ha-1impliesannual removal of about30 Pg of soil, a conservativetotal given the high erosionratesin partsof Africa, Latin America, and Asia [Oldeman et al., 1990; Pimentel,1993]. A disaggregated calculationusingspecificrates forNorthAmerica(17t ha-l),Europe (15t ha-1), Asia(35t ha-I exceptfor rice paddieswhereerosionis generallynegligible), Africa,andLatinAmerica (30t ha4 ) ended upwithabout 35Pg. endedup with a flux of about13 Tg N yr-1;thesecond one, With at least a quarter of this soil redepositedon adjacent 656 SMIL: NITROGENIN CROPPRODUCTION AN ACCOUNTOF GLOBALFLOWS croplandor on moredistantalluvia,the losswouldbe 22-25 Pg Indeed, the very notion of any direct, immediatebalancingof yr-1. SoilN content ishighlyvariable evenwithina single field, N inputsand removalson an annualbasisis misleadingas most ranging overanorderof magnitude (1.5-17t N ha-i ) in cropped of the addedN is not useddirectly by crops(or weeds):The bulk soils[Stevenson,1986]. A valuejust shortof 0.1% N is closeto the currentChinesemean [ Lindeft and Wu, 1996], while the U.S. of the nutrient recoveredby plantsbecomesavailable only after extensive turnover through the two opposing processesof averageis around0.125% [Sprent,1987].A conservative range of 0.08-0.1% N would meanthat 22-25 Pg of erodedsoil would immobilization and mineralization. Experiments using15N- carryawayabout20 (18-25)Tg N yr-1. labeled fertilizers are the best way to reveal this complexity:At the growing season'send, a large share (commonly up to 40%, sometimes more than 50%) of the fertilizer 1Nis immobilized in 4.6. LossesFrom Tops of Plants the soil's biomass,and the amount of (previously immobilized and then mineralized)soil N utilized by cropscan be 3-6 timesas Althoughrarelydiscussed, theselossesaddup to oneof the largestglobal N fluxes. They occur mostly within 2 or 3 weeks high as the nutrient drawn directly from the applied fertilizer after anthesis(full bloom), and at harvesttime the cropsmay [Stevenson,1986; Reddyand Reddy, 1993]. High C/N ratios of most crop residues,commonly above 50 commonlyhavebetween15 and30% lessN thanwastheirpeak and as high as 150, are particularly conducive to rapid 1N content.Neithertranslocation to rootsnor rootexudatesaregood immobilization. Some residual 1Nwill be bound in persistent explanations.A major part of the lossesmust be due to the sheddingof variousplant parts(pollen, flowers,and leaves), humus compoundsand be unavailableto plants for decadesor leachingof N from senescingleaves, and to heterotrophic centuries.How fast the short-livedfractionwill cycle dependson (microorganismic, insectand bird) grazing.All of theselosses the activity of microbial decomposers (which is highly (exceptfor windbornepollen) can be seenas merelyinternal temperature-and moisture-dependent)and on the availability of other sources of N. redistributions of N, asthelitterfall, leachingandherbivorywill returnthe nutrientto soils,and do not haveto be quantified. 5.1. Gains or Losses? Although bothreduced andoxidized N compounds areemitted by plant tops,mostof the N lossfrom topsof plantsis due to volatilization of NH3 [Francis etal., 1993]. Compai'isons ofmyminimum input andoutput estimates show an As with most other N losses, there is a considerable appreciablenet gain (8 Tg N); thoseof the two maximumvalues variability:Measuredpostanthesis lossesin wheatrangedfrom lessthan6 to 80kg N ha-l or fromlessthan8% to almost60%of showa smallnet loss(4 Tg N); cross-comparisons of minimum andmaximumestimates indicaterelativelylargegainsof 43 Tg N N presentat anthesis[Daiggeret al., 1976;Harper et al, 1987; yr-1(about 28kgNha-1) oranalmost aslarge loss of39TgN yr4 Kanampiuet al., 1997].Postanthesis declinesrangingmostly (about25 kg N ha-•). Thetwoextreme comparisons arenot Are then the world'scroplandsgainingor losingnitrogen'? between 20-50kgN ha-1 weremeasured in other cereal crops plausible:We have no indicationthat the world'sagricultural (rice,sorghum, andbarley),withdailylosses ashighas2 kg N soilswouldbeexperiencing a netgainor lossashighas40 Tg N eitherof thefirsttwopossibilities isentirely ha-1[Wetselaar andFarquhar, 1980], andFrancis etal. [1993] yr4. In contrast, astheyimplyannualincrements or removals of onlya foundratesashighas45-81kgN ha-1 fromcorn,equalto 52- plausible, wecannot exclude thepossibility of a 73% of all N unaccounted for by standardbalancecalculations. fewkgN ha-1. Although by improper agronomic practices Evenif thetypicallosswouldbejust 10kg N ha-i , theworld's smallbutchronicN losscaused naturalsoil degradation in manyfarming croplandswouldloseannuallysome15 Tg N, a flux similarto and by accelerated regions, thelikelihood of smallgainsappears to bemuchhigher. NO3-Nlosses dueto leaching. At20kgN ha-i, theglobal lossofaround 30TgN yr-1would An international comparisonof N balancesin almost 40 agroecosystems on threecontinents foundgainsin soilorganicN maketheN lossfromtopsof plantsaboutaslargea routeof N egress fromcroplands asdenitrification. Giventhemagnitude of this flux, it is imperative that all 1Nbalance studiesshould considerthis neglectedvariable before attributingany Table 6. Annual Balances ofN Flows intheWorld's Croplands Duringthe Mid- 1990s unaccounted lossesto unknownfactorsor to higherratesof denitrification or leaching[Kanampiuet al., 1997].Becausewe Flows Minimum Mean Maximum donotknowto whatextentthegaseous N losses fromtopsof Inputs l 51 143 85 169 165 85 186 190 85 I I 11 8 14 18 5 4 4 14 11 17 20 10 6 7 18 14 20 25 15 plantsmayhavebeencaptured by previously outlinedestimates Outputs ofNH3andNOx fluxes,I will assume thatnomorethan10(5-15) TgN yr-• arelostinthisway. 5. Nitrogen Balances Tabularrecapitulation of the estimatedinputsand losses (Table6) shows thatglobalcroplands receive169(151-186) Tg N yr-1andthatbetween 143-190 (mean ofabout 165)TgN yr-1 areremovedin harvested cropsanddueto a varietyof N losses. Harvested plants Losses NO emissions N2¸ emissions N 2emissions NH3volatilization NO3-leaching Soilerosion Losses fromtops of plants Figure1 showsthe fluxesinvolvedin globalcropproduction withina generalN cyclemodelcentered onplants.Thefactthat Balance +8 +4 -4 themeansof my conservatively estimated inputsandoutputs All values arein Tg N yr-l. Inputs arefromTable5;derivations of (169and165TgN) aremerely2%apartisnota strong indication individual output rates aredescribed inthetext.Allfigures arerounded to thatglobalagroecosystem is in N equilibrium. avoidtheappearance of unwarranted precision. SMIL: NITROGEN IN CROP PRODUCTION AN ACCOUNT OF GLOBAL FLOWS 657 NO, NO2 LU LIGHTNING•• N2 FOSSIL FUELS uJ •r• N20 NH3, NH• NO• FIXATION 115 FOOD DOMESTIC 23 ANIMALS PEOPLE FERTILIZERS FEEDING 6 78 23 17 DIGESTION 78 LOSSES FROM PLANT TOPS 10 CROP z ORGANIC RESIDUES WASTES 25 75 HARVESTED CROPS 85 RECYCLING 14 100 RECYCLING 18 5 ORGANIC MA'n'ER NO • IMMOBI LIZATIO N NITRIFICATION ONIFIC ATI ON NH3, NH4 .,..........••LEAC HI NG NO• •TRIFICATION [• EROSION 17 20 NO• •• • •, J ORGANIC '• MA'I-rER Figure 1. Simplifiedgraphof the biospheric nitrogencyclecenteredon agricultural crops.Only the storages (rectangles) andflows(valves)discussed in thispaperarequantified (all valuesarein Tg N yr-1). Thicklines identifyfluxesdirectlyaffectedby humanactions. (thepoolusuallycontaining > 90% of soilN) in almost60% of thecases,with a meanannualincrease of 35 kg N ha-1 andno of increasein the country's averageN applications, thereis no Netherlands, foundaverageannualaccumulations of 47 and38 long-term balance sheetsfor the RothamstedContinuousWheat doubtthatthesegainshavecontinued duringthe 1990s'My change in about1/3of thebalances [Floate,1978].In Europe, preliminary estimates putthemnowat about25 kgN ha-1 yr-I . tworecentnationalagricultural N balances, for Germany andthe Organicfarmingcanproduce the sameresults: Comparison of kgN ha-1, respectively [vanDijk,1993]. Zhu[1997]hasshown Experiment showthattheplotreceiving 35 t ha-I of farmyard thatnitrogen balance in China'sagriculture hasbeenpositive manuremorethandoubledits totalN soilcontentin 115years, between theearly1950sandthelate1980s. Giventherapidrate gainingthenutrientat anannualrateof about33 kgN ha-1, and 658 SMIL: NITROGENIN CROPPRODUCTIONAN ACCOUNTOF GLOBALFLOWS Suchgainsare not surprisinggiventhe oftenhigh ratesof N applicationsand the well-knownsequestration of a significant shareof the addednutrientin long-livedfractionsof soil organic matter. As many properly farmed soils aroundthe world are Assumingan average body massof 45 kg (weighted mean taking into account the age-sex structure of the world's population)and using typical lipid, bone and protein sharesin human bodies [Bailey, 1982] results in about 6 Tg N stored in bodiesof the world's6 billion people.With the globalpopulation growingannuallyby almost80 millionpeople,thenetincreaseof gaining annually 25-35kg N ha-1(thatis of theorderof 0.25- thispoolis lessthan80 Gg N yr-1, or merely0.3%of 23 Tg N 0.5% of total soil N stores), these increments could outweigh undoubtedN lossesfrom deterioratingsoils,particularlyin Africa consumedin food. More than 99% of ingestedN is thusexcreted, and advancingurbanization, as well as higher concentrationof meat, egg, and milk production,meansthat increasingsharesof this waste are released, directly or indirectly, into waters. Subsequentfate of this aqueousN rangesfrom benign(relatively rapid denitrification) to worrisome (nitrate contaminationof aquifers,coastaleutrophication). Another remarkable feature of anthropogenicN flows is the extent to which the nutrient is now moved amongcountriesand continentsby fertilizer and agriculturaltrade. During the mid1990s,about22 Tg N in inorganicfertilizers(more than a quarter of the applied total) were sold annually on the international market, and the traded farm products contained nearly 20% even the plot that did not receiveany N fertilizershad no longterm N loss [ Jenkinson, 1982]. where nutrientmining is most widespreador in highly erodible soilsof China'sLoessPlateau.Consequently, it is quitelikely that -1 the net resultis a nonnegligibleglobalN gain of 4-8 Tg N yr While this is welcome as far as the maintenance of the soil qualityis concerned, positiveN balancescarryrisksof increased N losses. Tracing major N inputs to the world's agroecosystems and subsequentN lossesassociatedwith food productionmakesit easierto answera key questionposedby Gallowayet al. [1995]: Where is N fixed by humansgoing?It also makesit possibleto suggestthe most effective ways of reducing the inputs of anthropogenic N into the biosphere. 5.2. Nitrogen Flows in Food Production My calculations show that almost half of all N received annuallyby the world'scroplands(46%, range43-50%) comes from syntheticfertilizers. This high dependenceis irreversible, and it is boundto increaseeven if the global population,as some forecastssuggest[UNO, 1998], were to stabilizeat a relatively low level (lessthan 10 billion people)duringthe nexttwo to three generations.While there are many energy sourcesthat can replace fossil fuels, whose combustion is the main cause of human alteration of carbon cycle, there appears to be no imminent alternativesto our high, and increasing,relianceon the nitrogenfixed by the Haber-Boschprocess[Smil, 1991]. Direct additionsof all newly fixed anthropogenicN, inorganic fertilizers (75-80 Tg N) and symbioticbiofixationby food, feed, andforagelegumes(22-32 Tg N), addedup to 105 (97-112) Tg N (almost10 Tg N yrq) of all N incorporated in foodandteed crops, mostly in cereals, oilseed cakes, and soybeans (FAOSTAT). The share of traded N will also increase in the future, as will the fraction of all N traded intercontinentally. 5.3. What' Can be Done? The best way to managethe continuinghuman interferencein N cycle is to maximize the efficiencies of N used in crop production.Fortunately,there are many realistic possibilitiesfor lowering the input of anthropogenicN in agriculturalproduction and for reducingits field and postharvestlosses[Munson and Runge, 1990; Fragosoand van Beusichem,1993; Dudal and Roy, 1995; van der Voet et al., 1996; Prasad and Power, 1997]. Soil testing,choiceof appropriate fertilizingcompounds, maintenance of propernutrientratios,andattentionto timingandplacement of fertilizers are the most importantdirect measuresof universal applicability.Indirect approacheswhich can either reducethe yr-• duringthemid-1990s. Asrecycling, in seeds, cropresidues, needfor syntheticfertilizersor increasetheefficiencyof theiruse rely primarily on greater contributions by biofixation and animal manures,and irrigation water returned38 (33-43) Tg N yr-1, humanmanagement wasresponsible for inputstotaling accomplished by morefrequentplantingof leguminous cropsor 143(130-155)Tg N yr-1andequaltoabout85%of allN received by optimizingconditionsfor otherdiazotrophs. by the world's agriculturalland. Natural atmosphericdeposition Improvinga varietyof agronomic practices, includingthose and no more than 1/3 of biofixation (by free-living bacteria and cyanobacteria)are the only inputs not directly manipulatedby humans. If the contributions from atmospheric deposition not directly connected with fertilization, can further reduce N attributable to NOx andNH3 fromcombustion andagriculture are integrated useof organicandsynthetic fertilizers,by minimizing soil erosion,by assuringadequatemoisturesupply,and by controllingpests.The valueof thisintegratedapproach hasbeen recognized by Codesof BestAgriculturalPracticemandated by theEuropean Union'sDirectiveof December1991anddesigned included, then more than 90% of all N received by the world's farmlandsoriginatein human activities. With 50% (46-56%) of all N inputs assimilatedby harvested crops, we have to accountfor 50% (44-54%) of addedN. Direct losses.Overall N uptake can be improvedby plantingNresponsive varieties,maximizingrecyclingof organicwastesand losses totheatmosphere (asN2,NOy,andNHx)addupto26-60 to protect fresh, coastal, and marine waters against nitrate Tg N, while 32-45 Tg N, or about 20-25% of all initial inputs, entergroundand surfacewaters.About50 Tg N yr-1 were removedfrom fields in harvestedcrops.SubtractingN in seeds(2 Tg N), postharvestlosses(5 Tg N), nonfooduses(1 Tg N), and animal feed (23 Tg N) leaves 17 Tg N (after 2 Tg N of retail and householdlosses)in plant foods.Adding 6 Tg N in animal foods (whose N comesnot only from concentratefeeds and cropland pasturesbut also from permanent grasslandsand, about 1 Tg, pollutionfrom diffusesources. Thesecodesrecommend thatapplications donotexceedcrop needs(after the contributionst¾omorganicsourcesare taken properly into account);thesecodesask that soils shouldnot be let bareduringrainyperiodsandthatnitratespresentin soilbetween cropsshouldbelimitedthroughplantingof trapcrops[seeIgnazi, 1996; and EFMA data]. fromaquatic catches) makesup23 Tg N yr-1 in theglobalfood Effectsof theseimprovements canbe impressive. El-Fouly and Fawzi [1996] concludedthat properN:P:K ratiosbasedon consumption. soil testingandplantanalysisandadjustedto the prevailing SMIL: NITROGEN IN CROP PRODUCTION AN ACCOUNT OF GLOBAL FLOWS cropping sequencecould raise typical Egyptian yields by 20% withoutusing more nitrogen.Gainsin fertilizer efficiencycould alreadybe seenin the U.S. recordsincethe early 1980s:Average yields of principal field crops have continuedto increaseat a fasterrate than the total applicationsof fertilizer N [Munsonand Runge, 1990; USDA, 1998]. Good agronomicpracticesshould raise the averageN use efficiency by at least 25-30% during the next two generations,i.e., to averageuptakesof at least50-55% in low-income countries and to around 65-70% in affluent nations. Even if the utilization of nitrogen from other sourceswould remain constant,suchhigher fertilizer efficiencieswould use 1012 Tg of the currently wasted N applications.In reality, an effective supply of nitrogen from organic wastes,biofixation, mineralization, and atmosphericdepositionshouldalso increase because of reduced N losses in soil erosion and because of more frequentrotationsand more vigorousrecycling.Again, relatively modestimprovementswouldtranslateinto impressivetotalgains: Reducingerosionallossesby 20% would saveroughly 4 Tg N from nonfertilizer sources,and expandingbiofixation, and waste recyclingby 10% would add another5 Mt N. Cumulativeeffects of adoptingwell-provenand mostly low-costmeasuresaimed at increasingefficiency of nutrient uptake would be then equal to expanding effective N supply tocrops by20-22Tgyr-1. These gains would make it possibleto satisfy virtually all anticipatedN demandneededto produceimprovingfood supply for the world's populationduring the next generationwithout increasingthe input of anthropogenic N in cropproduction.Such a stabilization would be the first step toward easingthe human impacton the biosphericN cycle. 6. Conclusions Of all the N flows involved in the world's crop production, only the inputs of the nutrient in inorganic fertilizers and N uptakeby cropsand their residuescan be quantifiedwith a high degreeof accuracy.For this reasonI presentedall N flows in the global agroecosystemas ranges rather than as single values. However, these extreme values do not represent the total uncertaintyin the estimates:They merely indicate a most likely range based on fairly conservativeassumptions.This makes it unlikely that actual biospheric flows would be lower than the lowestestimatespresentedhere. At the sametime, it is likely that in a number of cases, the real fluxes may be higher than the highest given estimates; indeed several published rates are outsidethe rangespresentedin Tables 5 and 6. With these caveats in mind, it appears that the world's croplands receiveabout170Tg of fixedN yr-l , withnearly9/10 of this total coming from managed, anthropogenic inputs. Cropping thus represents by far the most important human interference in the biospheric N cycle, far ahead of the combustionof fossilfuels. Only abouthalf of all fixed N reaching the fields is assimilated by crops and their residues; this conclusionis well supportedby numerousstudiestracing the recoveryof N in cropping. 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