From forest to waste: Assessment of the Brazilian soybean chain, usingnitrogen as a marker§

E.M.A. Smaling a,b,*, R. Roscoe c, J.P. Lesschen d, A.F. Bouwman e, E. Comunello c

a International Institute for Geo-Information Science and Earth Observation (ITC), P.O. Box 6, 7500 AA Enschede, The Netherlandsb Plant Production Systems, Wageningen University, P.O. Box 430, 6700 AK Wageningen, The Netherlandsc Embrapa Agropecuaria Oeste, Caixa Postal 661, Dourados, Mato Grosso do Sul, Brazild Alterra, Wageningen UR, P.O. Box 47, 6700AA Wageningen, The Netherlandse Netherlands Environmental Assessment Agency (MNP), P.O. Box 303, 3720 AH Bilthoven, The Netherlands

Agriculture, Ecosystems and Environment 128 (2008) 185–197

A R T I C L E I N F O

Article history:

Received 29 January 2008

Received in revised form 29 May 2008

Accepted 2 June 2008

Available online 25 July 2008

Keywords:

Soil fertility

Soybean

Soy meal

Nitrogen stocks and flows

Forest conversion

Conservation agriculture

Animal production

Human consumption

Waste

Brazil

China

European Union

A B S T R A C T

Soybean (Glycine max) is a booming crop in Brazil. In 2004, the export value was equivalent to 10 billion

US $, covering over 10% of total Brazilian exports. Three-quarters of total production leaves the country,

mainly to China and the European Union (EU). Soybean cultivation in Brazil is expected to expand further

in the coming decades, mainly responding to growing demand in Asia. This will, amongst others, entail

transport of vast amounts of nutrients, triggering the need to better study the entire soybean chain. The

objective of this study was to estimate and calculate the soybean chain, including five phases: conversion,

cultivation, transport and processing, consumption and waste disposal, starting in Brazil, and ending in

Brazil, China and EU, using nitrogen (N) as a marker, and looking at three time periods (1993–1995;

1998–2000; 2003–2005). The study revealed that conversion of forest and savanna to pasture and

agricultural land entails N losses of 2000–6000 million kg year�1. Removal of N in soybean harvests went

up from 1400 million to almost 3000 million kg year�1 between 1993–1995 and 2003–2005. These high

values were offset by biological N fixation by soybean and increased adoption of conservation agriculture.

N balances in soybean-based agricultural systems became positive after about one decade in the period

2003–2005, thus reducing the soybean-associated global N cascade. Upon crushing, three-quarters of

soybeans end up as high-protein soy meal, which is mainly fed to pigs and chickens. Nitrogen in meat,

milk and eggs from soy meal-fed animals was estimated at around 20% of N in freshly crushed soy meal.

More than half of the lost N can potentially be recycled, although mostly far away from the site of soybean

production.

� 2008 Elsevier B.V. All rights reserved.

Contents lists available at ScienceDirect

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1. Introduction

With economic growth, urbanization and changing diets, worlddemand for plant-derived oils and their derivates is soaring. Oilsare used inter alia in the food, feed and cosmetics industry, andincreasingly as a biofuel. Soybean is one of the major booming oilcrops. In addition to oil, it offers a very valuable by-product, i.e.protein-rich soy meal, a raw material for animal feed. Increasingglobal demand for animal products puts pressure on arable land,given the fact that at least two but often more kilograms of grainsare needed to produce one kilogram of meat, i.e. the so-called feed

§ This study was commissioned by the United Nations Food and Agriculture

Organization (FAO), Land and Water Development Division (AGL).* Corresponding author at: International Institute for Geo-Information Science

and Earth Observation (ITC), P.O. Box 6, 7500 AA Enschede, The Netherlands.

E-mail address: smaling@itc.nl (E.M.A. Smaling).

0167-8809/$ – see front matter � 2008 Elsevier B.V. All rights reserved.

doi:10.1016/j.agee.2008.06.005

meat ratio (Keyzer et al., 2005), and that an array of environmentalproblems is looming due to the expanding livestock sector (FAO,2006). The demand surge largely stems from China. Table 1 showsa ninefold increase in soy imports in 10 years, versus aninsignificant home production. This was triggered by China’s2002 WTO membership, which put an end to border tariffs andboosted trade (Van Berkum et al., 2006). Increasing demand hasbeen met with a supply response that is particularly strong inBrazil and Argentina. Country statistics show that in 2004,Brazilian production exceeded 50 million Mg, twice the amountrealized in 1997. Area and production increases were particularlystrong in the period 2001–2005, following a favorable devaluationof the national currency, the real. Soybean exports in 2004 earnedBrazil over 10 billion US $, against 4.2 billion US $ in 2000.

During the 1960s, soybean cultivation was concentrated in thethree states of the Southern Region of Brazil: Rio Grande do Sul,Santa Catarina and Parana. Later on, expansion to the CentralCerrado Region took place once varieties had been developed that

Table 1Soybean production, import and export for China (based on FAO statistics)

1994 1999 2004

Production (Mton) 15 15 17

Area (Mha) 10 9 10

Export (Mton) 540 214 346

Import (Mton) 2654 8236 24,863

Net import (Mton) 2113 8022 24,517

Source: FAO statistics.

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197186

were adapted to low latitudes. Currently, 60% of soybean pro-duction is concentrated in the Cerrado Region. The southern area ischaracterized by smallholder farmers, mostly organized incooperatives, whereas the central area is characterized by largeholdings, with very high levels of mechanization, and mostlyorganized in large private groups. In addition, climate is morestable in Central Brazil. The latest soybean expansion has takenplace in the northern Legal Amazon. Soybean production in theNorth represents only a small fraction of the currently plantedarea, but is expanding.

Recognizing that soybean (i) is a highly important commodityfor the Brazilian economy, (ii) contributes to the conversion offorest and savanna land, and (iii) travels long distances, ending up

Fig. 1. The phases of the l

in many different foods and feeds worldwide, there is a need tobetter understand the dynamics of the soybean sector, and howeconomic and environmental targets can be realized simulta-neously. In this study, nitrogen (N) is used as a marker. Theimportant role of N for life, for growth of crops and as an essentialelement in aminoacids/proteins in our food is obvious. The finaljudgment is about the trade offs between overloading and loss of Nversus the benefits in our food of plant and animal origin. Manystudies have looked into the N cycle and the flow of N in the foodsystem, at the global scale (Galloway and Cowling, 2002; Gallowayet al., 2004, 2007; Smil, 2002), or the national scale (e.g., Antikainenet al., 2005). In this paper we look more specifically into the role ofN from soybean in the food system. Soybean is a leguminous crop,capable of fixing atmospheric N through a symbiosis withRhizobium bacteria in the plant’s root nodules. Soybean cropstherefore receive no or very small amounts of N fertilizer as astarter.

The objective of this study is to quantify N stocks and flowsin and between the compartments of the Brazilian soybeanchain, and to find out where in the process N either remainsinside or disappears from the food chain. These compartmentsinclude forest and savanna conversion, soybean cultivation,transport and processing, animal and human consumption, andwaste disposal (Fig. 1).

arger soybean chain.

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197 187

2. Materials and methods

2.1. Spatio-temporal database

In Brazil, soybean is grown in large and small holdings, andboth as a monoculture and in annual rotations with maize, wheatand other crops. For characterizing the soybean farming systems,spatially explicit information was used. To show trends and avoidoutliers, average data were taken for the years 1993–1995, 1998–2000, and 2003–2005. Harvested area and production data wereobtained from municipality statistics (IBGE, 2006) and related tothe country-wide spatial municipality database (n = 5564 for2003–2005). Besides production data, several spatial data setswere necessary for the N balance calculation. Soil properties weretaken from 1:5-million-scale SOTER and WISE databases (FAOet al., 1998; Batjes, 2002; Batjes et al., 2004). Texture, bulk density,total N and total carbon content of the 0–20 cm soil layer wereincluded for calculation of the N balance. Rainfall data of the CRUTS 2.10 database were used, at a resolution of 0.5 degrees (Mitchelland Jones, 2005). For the calculation of erosion, the slope gradientwas required, which was derived from the GTOPO30 digitalelevation model (USGS, 1996), with a resolution of 3000 (approxi-mately 1 km). The maps were overlaid in a Geographic Informa-tion System, and the mean soil properties, rainfall and slope werecalculated for each municipality. The datasets allowed themapping of soybean land for each time period (Fig. 2a–c), as well

Fig. 3. (a–c) Distribution of the different soybean

Fig. 2. (a–c) Spatially explicit expansion of soybean area in B

as the particular system, i.e. soybean monoculture, soybean/maize and soybean/wheat (Fig. 3a–c).

2.2. Conversion

The expansion of soybean land happens at the expense ofpastures, which in turn farmers developed from Cerrado savannaand now increasingly from more densely wooded savanna. Data ondecreasing forest and savanna area cannot, however, be fullyexplained by soybean expansion. To calculate N flows underconversion regimes, a literature review was made. Removals of Nare in timber, firewood, in slash and burn of remaining above-ground biomass, and in soil and litter. Land clearing methods rangefrom selective cutting to the destructive savanna clearing system,where a correntao, a giant chain is attached between twobulldozers that move jointly, uprooting not only all vegetationbut also topsoil and litter. The totality of this material is thenburned (Van Gelder and Dros, 2005).

Mielniczuk et al. (2003) compared data on soil carbon inputsand stocks in long-term experiments in Sweden (Paustian et al.,1992) and in the South of Brazil (Lovato, 2001). In equilibrium, thedecomposition rate was 1.05% year�1 in the temperate soil and3.2% year�1 in the subtropical soil. The carbon to nitrogen ratio oforganic matter of Southern Brazilian soils is on average 12.5:1(Jantalia et al., 2006). A woodland savanna (Cerrado stricto sensu)stores 229 t of C ha�1 in biomass plus soil (1 m depth; Roscoe,

systems in Brazil for the period 2003–2005.

razil (averaged for 1993–1995; 1998–2000; 2003–2005).

Table 3Fertilizer N consumption (kg ha�1) by crop per region (after FAO, 2004b)

Region Soybeans Maize Wheat

North 2 10 0

Northeast 4 22 0

Central 7 40 9

Southeast 7 43 9

South 9 53 12

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197188

2005). Texture is also an important factor determining carbonstocks in Cerrados soils. Tognon et al. (1998) found a strong linearrelationship between texture and carbon stored in soil, varyingfrom 75–87 t of C ha�1 in sandy soil to 182–188 t of C ha�1 inclayey soils. Considering a C:N ratio of 12:1, this would representan N stock of about 7 t ha�1 in sandy soils and about 15 t ha�1 inclayey soils. Pastures normally develop higher soil N contents thanforest and savanna. Neill and Davidson (1999) showed that, from29 studies reviewed, 19 forest soils had increased their organicmatter content in surface when converted into pastures. Otherliterature data revealed that values for carbon in the upper 1 m ofBrazilian forest and savanna soils range from 100 to 200 t ha�1

(Matson et al., 1987; Cerri et al., 1991; Da Silva, 2004). Carbon invegetation ranged from 30–80 t ha�1 in savanna to 140 t ha�1 inforest (Graca et al., 1999). Total N losses in the forest systemfollowing clearcutting, based on review data by Matson et al.(1987) are in the order of 1000 kg N ha�1, but data from Cameroon(Kanmegne, 2004) and Madagascar (Brand and Pfund, 1998) showlosses as high as 3000 and 5000 kg ha�1 for forest. Bouwman(1995) found in La Selva, Costa Rica, soil C and N stocks of 81,000and 7600 kg ha�1, respectively. Soil N losses due to decompositionof soil organic matter following forest conversion to pasture were24% after 3 years, and after 5 years 40%. Schlesinger (1986) givesvalues of 21% loss of soil C when converting land from tropicalrainforest to agriculture (based on 19 sites). Based on this survey, itis assumed that forest and savanna have a ‘starting N stock’ invegetation and soil, whereas the situation prior to soybeancultivation is the ‘final N stock’, which is the input value for the‘Cultivation’ phase (Fig. 1). Pasture is considered an intermediatephase. Loss rates are then estimated on the basis of actualdeforestation data, and on the percentage loss that can beattributed to soybean expansion. Based on the literature study,and assuming a soil C:N ratio of 12:1, and a relevant topsoilthickness of 20 cm, an initial N stock in forest and savanna systemsof 8000–12,000 kg N ha�1 seems plausible, savanna being at thelower end and forest on the upper end. Moreover, it is assumed that25–50% of forest/savanna system N is lost in the process ofconversion to pasture and then to soybean.

2.3. Cultivation

2.3.1. Nutrient balance

The soybean system was analysed, largely using the NUTMONnutrient balance approach (Stoorvogel et al., 1993; FAO, 2004a;Lesschen et al., 2007). Table 2 lists the relevant flows. The nutrientbalance calculation involved a full cropping cycle of soybean(monoculture) or soybean + maize or wheat (rotation), and thecombined balance was thus calculated using the planted areas ofeach soybean system.

2.3.2. Tillage systems

Agriculture in the 1960s and 1970s in the South was heavilymechanized, leading to strong soil degradation (Mielniczuk et al.,2003; Jantalia et al., 2006). There was a widespread concept amongfarmers that well-managed soils would have completely clean and

Table 2Relevant N flows in soybean-based farming systems (Stoorvogel et al., 1993)

Inputs Outputs

IN1 Mineral fertilizer OUT1 Harvested crop parts

IN2 Organic inputs OUT2 Removed crop residues

IN3 Wet and dry deposition OUT3 Leaching

IN4 Biological N fixation OUT4 Gaseous losses

OUT5 Erosion

smooth surfaces, with residue incorporation and pulverized soils(Jantalia et al., 2006). Comparing the dynamics of soil organicmatter in a long-term experiment in the South of Brazil describedby Lovato (2001), Mielniczuk et al. (2003) estimated that no-tillagereduced the decomposition rate from 3.2% year�1 to 1.7% year�1. Inthe Cerrado region of Bahia State, Silva et al. (1994) sampled 220topsoils (0–15 cm) from soybean fields under conventional tillageand monoculture. The authors observed severe losses from 41%(clayey soils with>30% clay) to 80% (sandy soils with<15% clay) ofthe initial soil organic matter contents after 5 years of cultivation.However, Freitas et al. (2000) and Roscoe and Buurman (2003) didnot observe changes in the SOM stocks (0–40 cm) of a clayey DarkRed Latosol after 25 and 30 years of maize–bean successions withconventional tillage. Llilienfein and Wielcke (2003) reported nosignificant changes in C content of a clayey Oxisol after 12 years ofmaize–soybean rotation under conventional tillage. The presenceof a high-residue crop such as maize in these experiments maypartly explain the persistence of organic matter in these soils.However, the most important factor seems to be the highprotection of organic matter in clayey Cerrado soils, which arerich in iron and aluminum hydroxides (Resende et al., 1997).

2.3.3. IN1 Mineral fertilizer

The fertilizer use by crop study for Brazil (FAO, 2004b)estimated fertilizer consumption values per crop and per region(Table 3). These values were estimated for 2002 and weremultiplied with a correction factor, based on the relative differencebetween the fertilizer consumption of Table 3 and the IFA nationalfertilizer statistics for the calculation years 1993–1995, 1998–2000and 2003–2005. Total N consumption for these periods wasderived from the FAO fertilizer statistics, the values being1,148,600 Mg N for 1993–1995, 1,738,100 Mg N for 1998–2000and 2,415,400 Mg N for 2003–2004.

2.3.4. IN2 Organic inputs

Although Brazil has the largest livestock herd in the world, aswell as large numbers of pigs, sheep and poultry, application oforganic manures is limited to horticulture and perennial cropslocated close to the production sites. In the case of grain crops, theuse of organic fertilizers is not very common (FAO, 2004b).Therefore, the organic inputs for soybeans, maize and wheat wereset at zero.

2.3.5. IN3 Wet and dry deposition

Trebs et al. (2005) measured dry and wet N deposition for aremote pasture site in the Amazon Basin, and found 7.3–9.8kg ha�1 year�1. Krusche et al. (2003) also estimated an N depositionrate of about 9 kg ha�1 year�1. According to two chemistry transportmodels (Collins et al., 1997; Dentener et al., 2006), N deposition forBrazil amounts to 5–10 kg ha�1 year�1. Based on this, input throughN deposition was set at 8 kg ha�1 year�1.

2.3.6. IN4 Biological N fixation

Biological N fixation (IN4, kg N ha�1 year�1) is the mostimportant input for a leguminous crop such as soybean. Based

Table 4Percentage no-tillage per region, and per time-unit (after Roscoe, personal

communication)

Region 1993–1995 1998–2000 2003–2005

North 0 10 30

Northeast 0 10 30

Central 5 53 77

Southeast 21 74 85

South 21 74 85

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197 189

on studies of Zotarelli et al. (1998), Alves et al. (1999, 2005),Hungria et al. (2006) and Araujo et al. (2006), Rhizobium-based Nfixation by soybeans was set at 80% of the N in the above-groundplant parts. For non-symbiotic N fixation (based on the input byfree living bacteria), the following equation applies (FAO, 2004a):

IN4 ¼ 0:5þ 0:1�prainfall

2.3.7. OUT1 Harvested crop parts

Production and harvested areas for soybean, maize and wheatwere derived from the PAM (Agricultural Municipalities Production)database (IBGE, 2006). The N content of the harvested crop parts forsoybeans was set at 58 g kg�1 harvest product, based on studies byZotarelli et al. (1998), Alves et al. (1999, 2005), Hungria et al. (2006)and Araujo et al. (2006). For maize and wheat, the values of FAO(2004a) were used, i.e. 17 and 22 g kg�1, respectively.

2.3.8. OUT2 Removed crop residues

The removal of crop residues from the field is not a commonpractice in soybean farming systems in Brazil, as almost noalternative uses for them, such as stall-feeding, occur. Therefore,we assumed that all crop residues remain on the field and, therefore,OUT2 was set at zero.

2.3.9. OUT3 Leaching

For N leaching (OUT3, N in kg ha�1 year�1), the regressionmodel of De Willigen (2000) has been used:

OUT3 ¼ 0:0463þ 0:0037� P

C � L

� �� ðF þ D� NOM� UÞ

where P is the annual precipitation (mm); C the clay (%); L the layerthickness, i.e. rooting depth (m); F the mineral and organicfertilizer nitrogen (kg N ha�1 year�1); D the decomposition rate (%year�1); NOM the amount of nitrogen in soil organic matter(kg N ha�1); U the uptake by crop (kg N ha�1 year�1).

The first part of the regression equation determines whichfraction of mobile N will be leached, and the second part determineshow much mobile N is available. To prevent overestimation ofleaching, the first part of the equation was maximized at 1. In thecase of soybeans, only the uptake from the soil is taken into account(20%) and not the part which is derived from N fixation. For rootingdepth, values of Allen et al. (1998) have been used, which are 0.6 mfor soybeans, 0.9 m for maize, and 1.0 m for wheat. Decompositionrate was set at 3.2% year�1 for conventional tillage and 1.7% year�1

for no-tillage (Mielniczuk et al., 2003).

2.3.10. OUT4 Gaseous losses

The regression model developed by FAO (2004a) has been usedwith an additional factor for crop residues. NH3 volatilisation fromfield crop residues is set at 4%, which is the volatilisation rate ofsome ammonium-based fertilizers (Bouwman et al., 2002).

OUT4 ¼ ð0:025þ 0:000855� P þ 0:01725� F þ 0:117� OÞ

þ 0:113� F þ 0:04� R

where P is the annual precipitation (mm year�1); F the mineraland organic fertilizer nitrogen (kg N ha�1 year�1); O the organiccarbon content (%); R the nitrogen in remaining crop residues(kg N ha�1 year�1).

2.3.11. OUT5 Erosion

The RUSLE model was used (Renard et al., 1997), in combinationwith the spatial rainfall and soil data discussed in Section 2.1. TheRUSLE is expressed as:

A ¼ R� K � LS� C � P

where R is the rainfall erosivity factor (�); K the soil erodibilityfactor (kg m�2); LS the slope length and slope steepness factor (�);C the crop management factor (�) and P the erosion controlpractice factor (�).

The R-value was based on the annual erosivity map for Brazil byDa Silva (2004). The K-factor was based on the nomographs ofWischmeier and Smith (1978), but a simplified version was usedbecause of a lack of soil permeability and soil-structure data. The LSfactor was calculated using the slope gradient and a default slopelength of 22.13 m. According to Morgan (1995), the C-factor forsoybeans ranges from 0.20 to 0.50. As the C-factor is significantlyinfluenced by tillage, a distinction was made between conven-tional tillage and no-tillage. Erosion on no-tillage fields is onaverage only 25% of erosion under conventional tillage (Roscoe,unpublished data). As a consequence, a C-factor of 0.40 was usedfor conventional tillage and 0.10 for no-tillage. Table 4 gives thepercentages of agricultural area under no-tillage (Roscoe, unpub-lished data). Besides no-tillage management, no other erosioncontrol practices are used on a large-scale, hence the P-factor is 1.Finally, the loss of N was calculated by multiplying the annual soilloss by the soil N content and an enrichment factor, which was setat 2.3 (FAO, 2004a).

2.4. Transport and processing

Once harvested, the soybeans move in different directions(Fig. 4). The part undergoing processing inside Brazil (56%) iscrushed to produce soy oil and the protein-rich by-product soymeal. Upon crushing, the chain is only continued for soy meal, soyoil not containing N anymore. Then, 13% of the soy meal is used asfeedstuff in Brazil, whereas 30% is exported. Part of Braziliananimal produce is exported (4%). Further assumptions necessaryfor the calculations of N destinations are given in Table 5.

2.5. Consumption

For the (animal and human) consumption phase, a series ofassumptions was made relating to feed conversion efficiency inanimals, slaughterhouse efficiency, and human consumptioncharacteristics, including wasting of food. The N losses are in factnot all ‘losses’. Considerable percentages leave the ‘useful product’chain but can be recycled. This potential re-use is, however, oftenfar away from the site where soybeans are produced, hence causingan accumulation of N at consumption sites. The assumptions aresummarized in Table 6.

2.6. Human waste disposal

The final part of the chain looks into the human excreta. In ourcalculations we consider all N in human waste as potentialemission to the environment, excluding the N removed inwastewater treatment systems. This is because there is noquantitative information on the fate of the N for other systemssuch as latrines, septic tanks and other less institutionalized

Table 5Summary of the assumptions for ‘‘Transport and Processing’’

Process Remarks/reference

Starting N stock N in total harvested soybean for the three time intervals (‘‘Cultivation’’) constitutes the input N-value for ‘‘Transport and Processing’’

Transport and processing

losses

Seed use and transport losses between field and factory are estimated at 5%; losses during crushing and further transport are assumed

to be 5%. Total losses and seed use between the field and the livestock producers are thus 10%, which is consistent with estimates

from EMBRAPA (Maria do Rosario, personal communication)

Products following crushing Crushing beans is assumed to produce 20% oil, 75% meal, and 5% processing losses (weight percentages)

Import/export Based on the growing importance of China, it is assumed that in 1993–1995, 10% of exported soy went to China and 90% to EU,

whereas in 1998–2000 this ratio is assumed to be 30:70%, and in 2003–2005 50:50%

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197190

human waste disposal systems. For example in China, many of thehuman excreta have been recycled, and used to fertilizeagricultural systems until the late 1970s (FAO, 1977). However,it is not well known if this practice is still important at present (Zhuand Chen, 2002). Hence, by ignoring recycling of human excreta,we may overestimate the potential emission of human N to theenvironment.

Depending on the country, part of the population is connectedto sewerage systems, and part of the sewage water is treated inwastewater treatment plants. The N removal in treatmentinstallations depends on the type of installation. Assumptionsare summarized in Table 7.

2.7. Uncertainty analysis

An uncertainty analysis was applied to gain insight in theaccuracies and possible ranges of the results. For the cultivationphase, we followed the procedure of Lesschen et al. (2007), inwhich uncertainties were first calculated or estimated for eachflow at municipality level (Table 8). Since the results wereaggregated to regional and national level the uncertainties have tobe adjusted for spatial correlation. Spatial correlation occursbecause part of the input data is spatially dependent, e.g., soil andrainfall data. The spatial correlation coefficient was estimated foreach nutrient flow and ranged between 0 and 1.

Fig. 4. Destination of Braz

For Phase 3 (transporting and processing) and Phase 4(consumption), a simple sensitivity analysis was done by varyinga number of parameters by 25% and calculating the effect on thesoybean-derived human N intake.

3. Results

3.1. Conversion

Fig. 5 shows the cumulative area of deforestation, taken from theNational Institute of Space Research (INPE), and the total soybeanarea. The area increased from 11.3 million ha in 1993–1995, to 20.1million ha in 2003–2005. This increase occurred mainly in thecentral and northern regions. Until 2000, there is no relationbetween deforested area and soybean area, but between 2000 and2004, loss of forest is approximately equal to expansion in soybeanarea. In reality, the conversion rate of forest/savanna to pasture may,in these years, be approximately equal to the conversion ratebetween pasture and soybean land. However, these data do not fullyexplain whether most of the new soybean areas are savanna-derivedor forest-derived conversions. Also, soybean expansion has alwaystaken place in land under other arable crops as well.

Taking the rather constant deforestation rate of 2 millionha year�1 (Fig. 5), and attributing 50% of deforestation to soybeancultivation, N losses during Phase 1 are in the order of 2000–

ilian soybean (2004).

Table 6Summary of the assumptions for ‘‘Consumption’’

Process Remarks/reference

N conversion efficiency in pork

and poultry production

Soybean meal is assumed to be completely used in pork and poultry production. Conversion efficiencies (the percentage

of the N in feed that is converted to animal tissue) for Brazil and China are assumed to be 21% for pork and 34% for poultry

production. For EU, these numbers are 30% for pork and 34% for poultry based on Van der Hoek (1998). The complement of

the N conversion is excreted by the animals

N losses from animal manure Pork and poultry production is assumed to take place in stables. Ammonia (NH3) losses from animal manure in stables is

assumed to be 20% (Bouwman et al., 2002); further losses during the spreading of manure are not taken into account in this

analysis

Recycling of manure Recycling of pig and poultry manure as organic amendment in agriculture is assumed to be 80% in China and 90% in European

countries throughout the period covered by the analysis (Smil, 1999). For Brazil, we assumed that 10% of the manure is

not recycled

N in meat The N in the consumable meat is calculated from data provided by FAO (2007) on the live weight, dressed carcass weight,

retail cuts (52% of live weight for pork and 48% for poultry), and various edible offals (4% of live weight) and non-edible

by-products; edible by-products are assumed to be recycled, and non-edible by-products are assumed to be taken out of

the food cycle. Protein content of the meat (160 mg g�1 fresh meat for pork and 180 mg g�1 for poultry) and offals

(�180 mg g�1 for both pork and poultry meat) are from FAO (2007); that for bones (�50 mg g�1 for pigs and 30 for poultry)

is from Aerssens et al. (1998). Thus, total N in the live weight is distributed over consumable meat (82% for pork and 85%

for poultry) and offals (�7% for both pork and poultry)

Consumptive loss Consumptive loss is defined as the total loss in retailing and wholesaling and consumer and food service losses (from foods

forgotten and spoiled in the refrigerator to the uneaten food tossed in the garbage); based on inventories by Kantor et al.

(1997) and Bleken and Bakken (1997) these losses are substantial. For the USA, 15% of the meat is lost this way. For Europe,

we assumed a 10% loss, for developing countries 5%

Table 7Summary of the assumptions for ‘‘Human waste disposal’’

Process Remarks/reference

N excretion by population Total N excretion is calculated as total intake of N from soybeans through meat consumption. We accounted for N accumulation

in the growing human population. Population data are from FAO (2007)

Human wastewater to

sewerage and surface water

Fraction of the population connected to sewerage systems, and N removal in wastewater treatment systems were updated from

Bouwman et al. (2005)

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197 191

6000 million kg year�1 on the basis of the N losses presented inSection 2.2, with 1993–1995 at the lower and 2003–2005 at thehigher end of the range. It is difficult to attribute exactly theconversion to vegetation types and time periods, but it is obviousthat with the advance of soybean into the central and northernparts of the country, soybean expansion takes place increasingly atthe expense of forest.

Table 8Relative uncertainties as standard deviations for variables and N flows

Flow Variablesa

IN1 Fertilizer consumption (�10%)

Fertilizer use per crop (�50%)

IN3 Literature values ranging between 6 and 10 kg N/ha

IN4 Symbiotic N-fixation soybean (�10%)

and crop uptake (�22%)) 24%

Rainfall map (�20%) and regression (�50%)) 54%

OUT1 Crop production data (�20%)

N content crop products (�10%)

OUT3 Rainfall map (�20%) and clay content (�20%)) 28%

Fertilizer application (�51%), decomposition rate (�50%),

soil N content (�30%) and N uptake (�22%)) 50%

Regression model R2 = 0.67 (57%)

OUT4 Rainfall map (�20%), fertilizer application (�51%)

and organic carbon content (�20%)) 35%

Regression model R2 = 0.70 (55%)

OUT5 R: rainfall erosivity factor (�20%)

K: soil erodibility factor (�55%)

LS: slope and slope length factor (�50%)

C: crop management factor (�25%)

a Uncertainties in italic are educated guesses; other uncertainties were calculated ba

3.2. Cultivation

Soybean production data have been summarized in Table 9.OUT1 is given for the overall soybean-growing area, also includingoutputs in maize and wheat. The final row gives the total Nproduction through harvested soybeans, assuming N content inbeans of 5.8%. The uncertainty of the total amount of N from

Calculation Relative uncertainty (%)

Product 51

25

Summation 25

Product 22

Product and summation 81

Product and summation 65

Product 81

sed on available data.

Fig. 6. Aggregated soybean-system balances for Brazil.

Fig. 5. Cumulative areas for deforestation and soybean area increase since 1993.Fig. 7. Aggregated nutrient flows for soybean system in Brazil for the period 1998–

2000.

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197192

soybean production is only 7%, based on the 22% uncertainty forOUT1 and a spatial correlation factor of 0.3.

N flows were calculated for the different regions and differentsoybean farming systems portrayed in Figs. 2 and 3. Fig. 6 showsthat surface N balance deficits decrease with time and becomesurpluses, primarily because of the increased importance of no-tillage, reducing leaching and erosion. Average uncertainty ofthe N balance is �9 kg N ha�1, ranging between �6 kg N ha�1 forthe Southeast region and �16 kg N ha�1 for the North region ascalculated for the 1998–2000 period. Soybean is estimated to fix 80%of its needs, and since the crop residues remain in the field, the valuesof OUT1 and IN4 are about equal (Fig. 7). Based on the total soybeanarea and N balances calculated for the three time periods in the‘‘Cultivation’’ phase, there is a total loss of 182 million kg N year�1 in1993/1995, a loss of 15 million kg N year�1 in 1998/2000, and a gainof 62 million kg N year�1 in 2003/2005.

3.3. Transport, processing and consumption

Based on the assumptions listed in Tables 5 and 6, flows werecalculated during processing, transport and animal and humanconsumption. Fig. 8 shows the values and flows representing therelevant processes for the three periods. Starting stocks correspondwith values given in Table 9, i.e. the output of ‘Cultivation’. About

Table 9Summary of soybean production data

1993–1995 1998–2000 2003–2005

Harvested soybean area (million ha) 11.3 13.4 20.1

Soybean yield (Mg ha�1) 2.16 2.37 2.53

OUT1—crop products (kg N ha�1) 101 115 122

Total soybean N (in 1000 Mg) 1420 � 94 1843 � 122 2949 � 195

20% of total N entering Phases 3 and 4 ends up as animal productsthat are consumed by humans. This percentage decreased slightlybetween 1993–1995 and 2003–2005 (from 21.1 to 19.8%). Inaddition, Table 10 shows total N ingested by humans per country/region. Adding up the rows gives totals of 300, 377 and 583million kg N year�1 for the three periods.

Table 11 provides a sensitivity ranking for Phases 3 and 4, i.e., onfinal soybean-derived N intake from meat due to variation of thedifferent input parameters by +25%. It is clear that the feed Nconversion in livestock production is the major uncertainty inPhases 3 and 4. This is related to the large fraction of soy meal thatgoes into livestock production, and the generally low efficiency offeed conversion to meat.

3.4. Waste disposal

Table 12 shows the fate of consumed N. Total consumption(583 million kg N year�1) is the output value of Phase 4 for2003–2005. European Union (EU) households have by far thelargest percentage of sewerage connections (84%). However,even with advanced wastewater treatment in Europe with 51.5%of N in influents being removed, 48.5% of the N entering sewagesystems still reaches surface waters. If we consider all house-holds in the EU including those lacking sewage connection,57% of the soybean N consumed is not removed in wastewatertreatment.

In Brazil and China less than 10% of the soybean N is removedfrom sewage water, hence more than 90% is not treated and is apotential emission to the environment, since far fewer householdshave a sewerage connection than in the EU. The fate of N in non-sewerage outlets, ranging from latrines to septic tanks, has notbeen considered explicitly due to lack of data. Human excretathat are collected may be used to fertilize agricultural fields,particularly in China. Hence, the potential N emission to theenvironment may be an overestimation.

4. Discussion

4.1. Limitations of the study

Given the booming market, expansion of the soybean areain Brazil seems economically viable, but it has a social andenvironmental price. Many negative externalities of the soybeansector are not covered in this study, including plant and animalbiodiversity loss, carbon emissions, changing air circulationand increased drought occurrence, unlawful land acquisition,forced migration of forest inhabitants, rural poverty and lowemployment rates.

Fig. 8. (a–c) Nitrogen flows in Phases 3 and 4 in Gg N year�1: N in food, N for recycling, and N lost to the environment.

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197 193

Table 10Nitrogen consumed in Brazilian soybean-derived animal products (output of Phase

4; in million kg N year�1)

Brazil China EU

Poultry Pork Poultry Pork Poultry Pork

1993–1995 57 13 6 13 78 134

1998–2000 74 16 23 50 79 135

2003–2005 118 26 61 134 90 154

Table 12Fate of the Brazilian soybean N in meat consumed by humans in Brazil, China and

EU (in million kg N year�1, in 2003–2005)

Brazil China EU Total

Consumption 144 195 244 583

Population change (% year�1) 1 1 0

N excretion 142 193 244 580

Connection to sewerage (%) 44 19 84

Removal in wastewater treatment (%) 18 10 51.5

N emission (potential, see text) 131 189 138 459

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On ‘Conversion’, studies exist that look at vegetation carbon,and at soil carbon available in forest and savanna. Fewer look at N,let alone both vegetation N and soil N. Some studies take soil Ndown to a depth of 1 m, others just consider 0–20 cm. Land can becleared in many different ways. The fully fledged bulldozer-assisted clearing of cerrado mentioned by Van Gelder and Dros(2005) is much more destructive than the selective cutting thattakes place elsewhere. For this study, ‘clearcutting’ is consideredto take place, although the actual process may include periods ofpartial clearing as well as periods under pasture, which oftenshow increases in soil C and N over time, particularly whenmanaged well.

On ‘Cultivation’, N is clearly not a limiting factor as soybean is aleguminous crop, but other nutrients may well be or becomelimiting. FAO (2004b) shows that soybean in Brazil normally doesreceive P and other fertilizers, next to tiny amounts of N. Theseother nutrients are not considered in this study. No attention ispaid either to the fact that, currently, most soybean varieties aregenetically modified (Brazilian Ministry of Agriculture estimatesare 70% of the soybean area under GM soybean in 2005/2006), andbased on ‘Round-up ready’ herbicide use, which are imperative foradopting minimum tillage practices. A social externality not takeninto account is that the labour/land ratio of large-scale soybeanproduction in central Brazil is very low (1 on 400 ha) comparedwith small-scale agriculture in the south (80 on 400 ha) (VanBerkum et al., 2006).

Another issue outside the scope of the current study is theincreased use of soy oil as a biodiesel. A new market was opened tosoybean oil in 2006/2007 as a consequence of the BrazilianNational Biodiesel Programme. The programme has allowed theinclusion of 2% of biodiesel in the diesel from petroleum sinceJanuary 2006. This proportion will become compulsory in 2008and will be increased to 5% in 2013. The demand for vegetable oil in2008 is estimated about 1 million t and, in 2013, 2.5 million Mg.According to Petrobras projections, in 2008, the demand forvegetable oil in this process will be about 500,000 Mg. Therefore,the energy sector will absorb about 1.5–3.0 million Mg of vegetableoil in the coming 2–5 years.

On ‘Transport’, a recently opened port in Santarem and thecompletion of the road between Cuiaba and Santarem opens up

Table 11Sensitivity of final soybean-derived N intake from meat due to variation of the differe

Parameter Change of N in

Transport/processing loss �2.6

Fraction production to industry within Brazil +1

Fraction consumption of processed beans in Brazil �1.5

Fraction export of meal to Europe vs. China +2.1

Use of soybean meal for pigs vs. poultry �6

N conversion pigs +13.5

N conversion poultry +11.5

Fraction offals edible �2.1

Fraction non-edible offals �2.7

Fraction retailing, wholesaling and household food waste �2.7

new opportunities for agricultural development, but it may equallypose substantive social, environmental and production risks. VanBerkum et al. (2006) show that export and import figures can differmarkedly. For example, ITC/WTO data show that on soy meal tradebetween Latin America and The Netherlands, Brazil exported 4million Mg of soy meal, but The Netherlands only imported 1.3million Mg. Similarly, Argentina export data show 2.3 million Mgshipped to The Netherlands, but the Dutch statistics showimported soy meal from Argentina to have amounted to just over1.1 million Mg. Although ships do at times change destination (e.g.to France, Belgium or Germany) while moving overseas, thedifferences are significant.

On ‘Consumption’, there are several causes of uncertainty. Themost uncertain parts of the consumption chain are the feed Nconversion in livestock production systems and food spoilage andwaste. The process that determines a large part of the N loss fromthe soybean chain is the feed conversion. A small variation causes alarge deviation in the end results (Table 11). Estimates for feed Nconversion are from large-scale studies, and differences betweenthe estimates for Brazil and China (21% efficiency for pigs) andEurope (30%) indicate that management has an important effect onN lost from the soybean chain. The results shown here showgreater efficiency of N capture by animal production than reportedpreviously (Smil, 1999, 2001). In the previous analysis, the effect ofN recycling within the system was not considered, and older datawere used to estimate the efficiency of feed N utilization byanimals. Since livestock production systems are rapidly changing,particularly in developing countries, where modern units withhigh levels of management replace existing ones, efficiencies mayalso increase rapidly in countries like Brazil and China.

In our study roughly 20% of the N in the soybeans is actuallyconsumed as meat by humans. Since we consider only pork andpoultry, our estimate exceeds the 14% estimated by Smil (2002) forall livestock including milk and beef cattle.

Estimates of food availability for human consumption fromfood balance sheets are generally used as an approximate level offood actually consumed. This may work reasonably well indeveloping countries, but in developed countries this approachcan overstate the level of consumption because the amount of foodspoilage and waste in catering establishments is rather high. The

nt input parameters by +25%

take (%) Remarks

More export of meal, with on the average higher efficiency

More export of meal, with on the average higher efficiency

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197 195

amount of food actually consumed may be lower than the quantityshown in the food balance sheet depending on the degree of lossesof edible food and nutrients in the household, e.g. during storage, inpreparation and cooking (which affect vitamins and minerals to agreater extent than they do calories, protein and fat), as plate-waste or quantities fed to domestic animals and pets, or thrownaway. Household survey data may prove useful in such instancesfor adjusting the waste component in the food balance sheet.

On ‘Waste Disposal’, other defecation destinations than sewerageand water treatment are not explicitly dealt with in this study. Theymay be equally or more constraining to public health, but canbe considered as potential emissions of N compounds into theenvironment.

Quantification of the fate of the N that is lost from the chain andassessment of the environmental impact is outside the scope ofthis paper. This would require a completely different approach likelife cycle analysis (LCA). In actual fact, results of our study mayserve as a basis for LCA of the soybean food chain. In this respect,the intention is also not to provide an exhaustive overview of Nstocks and flows as was done for Finland by Antikainen et al.(2005).

4.2. Opportunities to make the chain more sustainable

Major reductions in N losses are possible in Phases 1, 4 and 5(Fig. 1). Although no research was done on solutions, someopportunities stand out that may contribute to striking a moresustainable balance between economic and environmental goals.

On ‘Conversion’, improvements and solutions are more in thefield of forest management policies, law enforcement, and humanrights protection than in agronomy. Payment for environmentalservices along the lines of Kyoto Protocol mechanisms may be away to harmonize economic, environmental and social goals atnational and local scale.

As to ‘Cultivation’, Brazil’s National Agricultural ResearchInstitute (Embrapa) has indicated that considerable strides canstill be made to raise productivity on existing soybean land, tofurther spread the practice of no-tillage, to restore and cultivatedegraded pastures, and to rotate pastures and soybean. Estimateson ‘degraded’ land that could be converted to soybean are between10 and 30 million ha.

Although trade generates economic benefits, soybeans and soymeal face ‘Transport’ over very wide distances before entering theconsumption cycle. Atmospherically fixed N from Brazil ends up indung piles in Western Europe and China. In the Netherlands, forexample, this has for some decades now been regarded as a majorenvironmental problem.

The consumption chain in the EU (soy meal–animal feedsector–farms–slaughterhouse–supermarkets) is increasingly ver-tically integrated. This makes the sector more efficient, but also amore powerful force vis-a-vis producers and consumers. Reducedconsumption of animal products is a way to reduce the tension onthe soybean chain. Although not desirable from an economicviewpoint, livestock production with a 20–30% N conversion isquite inefficient when converting plant N to proteins in meat, milkor eggs. Price regulations and campaigns to influence consumerbehavior represent a possible way to change human diets.

On ‘human waste disposal’, research and dissemination of goodhygienic practices can help in keeping excess N out of surfacewaters.

On a more general note, the instrument of round tables is usedwith some degree of success, both for oil palm as well as forsoybean. The Round Table on Responsible Soy includes private andpublic sector stakeholders from Brazil and export countries, socialand environmental NGOs, and forest inhabitants. In The Nether-

lands, a ‘Soy Coalition’ has managed to table the adverse social andenvironmental aspects of soybean production in parliament.Some major food industries have decided to track and trace soymeal using more specific and measurable indicators to ascertainthey are selling products grown in a socially and environmentallybenign way.

5. Conclusions

1. B

razil is a major soybean producer and exporter and is expectedto become even more powerful. In 1993–1995, 1998–2000,2003–2005, soybean production in Brazil was 24.4, 31.8 and50.8 million Mg, respectively. About 75% is exported. Soybeanexports cover 10% of the country’s total export income; EU andChina are major importers.

2. S

oybean is grown in monocultures on very large farms(>1000 ha) in the Central parts of the country, and on familyfarms in the South, in rotation with maize and wheat. In theNorth, soybean cultivation is relatively new. The Central partnow is the major producer, having overtaken the Southern partin the past 5 years.

3. A

mazon forest and Cerrado savanna has most often beenreplaced by pastures. These are increasingly replaced bysoybean farms. Some parts of the Amazon are converted intosoybean fields directly. Soybean has also replaced other arablecrops. Its growth can partially be linked to forest and savannaremoval.

4. E

stimates (Phase 1) of N losses in forest and savanna that can beattributed to soybean range from 2000 to 6000 million kg ofN year�1. This comes on top of biodiversity loss, destruction ofliving areas, and the creation of increasingly dry conditions dueto reduced air circulation on the continent.

5. E

stimates (Phase 2) of N losses in soybean fields were182 million kg of N year�1 in 1993–1995, but in 2003–2005,there was a gain of 62 million kg of N, due to generally improvedpractices of conservation agriculture, and due to the N-fixingnature of (the leguminous species) soybean. Other nutrientsmay be limiting, and/or have negative nutrient balances (P, Kand trace elements), but this was not investigated. In addition,the issues of genetically modified soybean (currently estimatedat 43%) and the massive use of pesticides and associated healthrisks have not been dealt with here.

6. O

f the total soybean production, 75% is turned into soy meal, 20%into soy oil, and about 5% is lost during processing and transport.As soy oil contains no N, it is no longer relevant for the chainstudied here. The soy meal is largely fed to animals, mainly topigs and chickens.

7. D

uring animal production and human consumption, a series ofN losses come to the fore, production of animal manure beingthe main (recyclable) loss. The N remaining in consumed meatfor humans is about 20% of the N available in the harvestedsoybeans.

8. O

f the N excreted by humans into sewerage systems, 79% isemitted into the environment, whereas the complement isremoved from wastewater by treatment.

Acknowledgements

This study has greatly benefited from the guidance of JanPoulisse (FAO, Land and Water Development Division). EdilbertoSena (Frente em Defesa da Amazonia, Santarem), Siemen vanBerkum (LEI, The Hague), Jan Maarten Dros (AIDEnvironment,Amsterdam) and several colleagues of the Brazilian NationalAgricultural Research Organization (Embrapa) in Dourados, Brazil,

E.M.A. Smaling et al. / Agriculture, Ecosystems and Environment 128 (2008) 185–197196

are all gratefully acknowledged for providing help and feedbackwhile this study was conducted.

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