Water Quality report (Essay) APA format three pages four citations

profiletamber92
fertilizer.pdf

Essay

Fertilizing Nature: A Tragedy of Excess in the Commons Allen G. Good, Perrin H. Beatty*

Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

Abstract: Globally, we are apply- ing excessive nitrogen (N) fertilizers to our agricultural crops, which ultimately causes nitrogen pollu- tion to our ecosphere. The atmo- sphere is polluted by N2O and NOx gases that directly and indirectly increase atmospheric warming and climate change. Nitrogen is also leached from agricultural lands as the water-soluble form NO3

2 ,

which increases nutrient overload in rivers, lakes, and oceans, causing ‘‘dead zones’’, reducing property values and the diversity of aquatic life, and damaging our drinking water and aquatic-associated in- dustries such as fishing and tour- ism. Why do some countries show reductions in fertilizer use while others show increasing use? What N fertilizer application reductions could occur, without compromis- ing crop yields? And what are the economic and environmental ben- efits of using directed nutrient management strategies?

In his 1968 seminal paper, ‘‘The

Tragedy of the Commons,’’ the late

Garrett Hardin argued that individuals,

acting in rational pursuit of their own self-

interest, will sacrifice the long-term viabil-

ity of a shared resource for short-term

gain. ‘‘Ruin is the destination toward

which all men rush, each pursuing his

own best interest in a society that believes

in the freedom of the commons.’’ In the

case of pollution, he wrote, ‘‘Here it is not

a question of taking something out of the

commons, but of putting something in –

sewage, or chemical wastes into water’’

[1]. Perhaps one of the best examples of

this ‘‘over-contribution’’ is nitrogen (N)

fertilizers, where individual rational be-

haviour (i.e., applying high fertilizer rates

to maximize short-term economic yield)

can cause long-range harm to the envi-

ronment. The true cost of applying high

rates of N fertilizers in order to maximize

overall yield is already apparent in the

form of global climate change. The

incentive to over-apply N fertilizers is

likely to continue, as both the Food and

Agriculture Organization (FAO) and the

United Nations (UN) have predicted high

future demand for cereal production,

especially within the developing nations,

due to predicted increases in populations

and dietary shifts.

In developed countries, crop yields have

nearly reached their biological maximum

and increasing fertilizer use is unlikely to

provide any significant additional gains. In

contrast, in developing countries, there is

still a large yield gap. Although we need to

increase crop yields to feed the growing

global population, we also need to do this

in an environmentally sustainable way.

We cannot increase our yields by increas-

ing N fertilizer application (not even in

areas of the world that still have an

exploitable yield gap) at the expense of

the ozone layer or marine life. Certainly,

while regions with an N balance surplus

can reduce N fertilizer application rates

without yield losses (i.e., Denmark), other

regions will need to increase their N use

(i.e., sub-Saharan Africa), but still use best

management practices. N balanced coun-

tries may also be able to reduce N fertilizer

rates without yield loss by employing new

technologies such as improved plant

varieties, region-specific farming practices,

time-release N fertilizer, drip irrigation,

crop rotation, bioinoculants, and similar

approaches.

Nitrogen Is a Key Aquatic and Atmospheric Pollutant

Nitrogen is the key limiting nutrient for

most crops and many aquatic and

terrestrial ecosystems. Unfortunately, the

massive increase in anthropogenic N

introduced into the environment, largely

via N fertilizers, has had significant

negative environmental consequences

[2,3]. The link between agriculture and

nitrate pollution is well established with

impacts on drinking water [4,5] and the

eutrophication of fresh water and marine

ecosystems, including the proliferation of

harmful algal blooms and ‘‘dead zones’’

in coastal marine ecosystems [6]. For

example, in the United States, 89% of

total N inputs into the Mississippi River

come from agricultural runoff and drain-

age [6]. In addition, agriculture plays a

substantial role in the balance of the

three most significant anthropogenic

greenhouse gases (GHGs): carbon diox-

ide (CO2), nitrous oxide (N2O), and

methane (CH4). The global warming

potential (GWP) of these gases can be

expressed in CO2 equivalents. The

GWPs of N2O and CH4 are 296 and 23

times greater, respectively, than a unit of

CO2 [7]. Of these, N2O is the most

important gas emitted by fertilizer use,

because of its large CO2 equivalent

influence on GWP. In the US, agriculture

contributed 68% of the country’s N2O

emissions in 2009, but only 3.6% of the

total US GHG emissions [8].

Essays articulate a specific perspective on a topic of broad interest to scientists.

Citation: Good AG, Beatty PH (2011) Fertilizing Nature: A Tragedy of Excess in the Commons. PLoS Biol 9(8): e1001124. doi:10.1371/journal.pbio.1001124

Published August 16, 2011

Copyright: � 2011 Good, Beatty. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This research was funded by grant #2009C001R from the Alberta Crop Industry Development Fund (http://www.acidf.ca/).The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

Abbreviations: BNMP, best nutrient management practices; CAP, common agricultural policy; CT-CC, conventional tillage and continuous corn; EEONR, environmental and economical optimal N rate; EONR; economical optimal N rate; EU, European Union; FAO, Food and Agriculture Organization; GHG, greenhouse gas; GWP, global warming potential; MRTN, maximum return to N; N, nitrogen; NUE, nitrogen use efficiency; UN, United Nations; 4R, right source, right time, right place, right rate.

* E-mail: [email protected]

PLoS Biology | www.plosbiology.org 1 August 2011 | Volume 9 | Issue 8 | e1001124

Table 1. The N fertilizer costs and consumption of specific countries for past use and future forecasts.

World EU Denmark China

Year

Price

($ Mton-1) Total Consumption (MMt N)

Value

(US$B)

Total Consumption (MMt N)

Consumption (kg ha21)

Total Consumption (MMt N)

Consumption (kg ha21)

Total Consumption (MMt N)

Consumption (kg ha21)

1987 425 75.8 $32.2 30.3 127 0.367 142 18.6 138

1997 610 81.3 $49.6 15.5 101 0.238 120 25.4 185

2007 795 100.6 $80.0 13.3 114 0.172 75 34.8 247

2012 869 103.2 $89.7 13.0 114 0.170 74 37.6 267

2020 a

980 110.7 $108.5 13.0 114 0.170 74 42.4 302

2030 b

1220 126.9 $154.8 13.0 114 0.170 74 54.5 388

2050 c

1500 151.6 $227.4 13.0 114 0.170 74 69.0 487

Italicized text represents future estimates and are based on no increase in consumption (EU and Denmark) or a linear increase in consumption, equivalent to the rate of increase between 1987 and 2007 (world and China) (http://www.fao.org/corp/statistics/; accessed 16 June 2010). aEstimates of World N consumption in 2020 are 110 MMt [55], 112 MMt [56], and 135 MMt [57]. b

Estimates of World N consumption in 2030 are 125 MMt [56]. c Estimates of World N consumption in 2050 are 135 MMt [58] and 236 MMt [57].

MMt, million metric tons. doi:10.1371/journal.pbio.1001124.t001

Table 2. Total N consumption, economic, and environmental costs for the US, China, India, and the world.

Year

Actual/Predicted Consumption (MMt N)

Value

(US$B)

Proposed Reduction (from 2007)

Reduced Consumption (MMt N)

Excess N Applied (MMt N)

Value

(US$B) CO2 GWP (MMt)a

CO2 GWP Value

(US$B)

Environmental Cost

(US$B)

World

1987 75.8 32.2

2007 100.6 80.0

2020 110.7 108.5 10% 90.5 20.2 19.8 94 1.4 8.7

2030 126.9 154.8 20% 80.5 46.4 56.6 215.8 3.2 24.9

2050 151.6 227.4 20% 80.5 71.1 106.7 330.7 5.0 46.9

US

1987 9.5 4.1

2007 14.5 11.5

2020 16.7 16.3 5% 13.8 2.9 2.7 13.5 0.2 1.2

2030 19.9 24.3 10% 13.0 6.9 8.4 32.1 0.5 3.7

2050 23.5 35.2 10% 13.0 10.4 15.7 48.4 0.7 6.9

China

1987 18.6 7.1

2007 34.8 27.6

2020 42.4 42.0 10% 31.3 11.5 11.3 53.5 0.8 5.0

2030 54.5 66.5 20% 27.8 26.7 32.5 124.2 1.9 14.3

2050 69.0 103.5 20% 27.8 41.2 61.7 191.6 2.9 27.1

India

1987 5.7 2.4

2007 14.4 11.5

2020 19.1 18.7 10% 13.0 6.1 6.0 28.4 0.4 2.6

2030 24.7 30.2 20% 11.5 13.2 16.1 61.4 0.9 7.1

2050 31.4 47.1 20% 11.5 19.9 29.8 92.6 1.4 13.1

Economic costs are calculated based on the current and predicted cost of N fertilizer. Environmental costs are equal to 44% of the value of the excess N applied. a The GWP of N2O based on a 1% of excess applied N being lost as N2O-N; excess N applied MMt N x 0.016(44/28) x GWP of N2O (296). CO2 GWP Value (1 Tonne CO2 = US$15). Price of N fertilizer (1987 = US$425; 2007 = US$795; 2020 = US$980; 2030 = US$1,220; 2050 = US$1,500).

doi:10.1371/journal.pbio.1001124.t002

.

PLoS Biology | www.plosbiology.org 2 August 2011 | Volume 9 | Issue 8 | e1001124

Rather than try to fix the consequences of

N fertilizer overuse, a better solution would

be to employ better management strategies,

such as tillage type, rate and timing of N

fertilizer application, better sources of N

fertilizer such as timed-release N fertilizer,

bioinoculants or biological N fixation, and

more N-efficient crop plants. Although

reducing or eliminating anthropomorphic

N pollution will necessitate a multi-dimen-

sional approach, we will focus mainly on one

approach, N fertilizer application reduction.

Table 3. Improvements in nitrogen use efficiency in crop plants during field trials.

Crop Year

N Fertilizer Rate (kg N ha

21 )

% Decr. in N Fertilizer

% Incr. in Yield PFPN

a % Incr. PFPN

a N Management Ref.

High Low From High Rate

From Low Rate

Americas

Maize 2000–03 191 0 60 55 72 31 BMP versus Illinois state averages

[49]

Maize 1980–00 145 0 35 42 57 36 Improved BMP and use of modern hybrids

[36]

Wheat 1994–96 250 180 28 21 20 34 67 Farmers’ practice versus BNMP in Northern Mexico

[59]

Barley 2007 169 107 37 NC b

46 71 54 Field trials in Alberta, Canada

[46]

Maize 1998–99 250 187 25 NCb 43 57 33 Improving N management Kansas & Nebraska, US

[60]

Maize 2001–03 134 101 25 NCb 50 67 34 Michigan, N2O emissions double after using more N than the low rate

[37]

Maize 2007–08 180 135 25 NC b

44 59 25 Michigan, using the lower N rate reduces N2O emission by 44%

[38]

Maize 2005–07 150 90 40 28 c

69 105 34 Eastern Canada, N2O emission at low N rate were half that of high N rate

[41]

Europe

Wheat 2003–07 200 174 13 1 27 30 11 High rate versus optimal N rate at the N:grain price ratio = 5

[42]

Cereals 1985–02 na na na 36 44 22 Average UK cereal NUE declining use of N fertilizers

[61]

Wheat Prior to 2001 200 160 20 NC b

52 64 24 Using balanced nutrients, ‘‘Law of Minimum’’

[13]

Asia

Rice 1987–99 108 76 30 NCb 45 66 47 Fertilizer rate reduced, NUE variety in Japan

[62]

Rice 1998–99 167 133 20 8 37 49 32 FFP versus SSNMd at 21 farms in China

[63]

Rice 1997–99 117 112 4 7 49 52 6 FFP versus SSNMd at 179 sites in Asia

[33]

Rice 2003–06 300 200 33 3 27 41 52 East China farmers’ N practice versus opt N fertilization

[18]

Rice 1995–98 70 53 24 NC b

30 40 33. On-farm studies, increasing plant population density

[32]

Wheat 2003–06 325 128 61 5 18 47 161 North China Plain farmers’ N practice versus opt N fertilization

[18]

Maize 2003–06 263 158 40 5 32 56 75 North China Plain farmers’ N practice versus optimum N fertilization

[18]

aPFPN, kg grain per kg kg N applied. b

NC, no change in yield. c Slight decrease in yield at the low N fertilizer rate versus high N fertilizer rate.

dFFP, farmers’ fertilizer practice; SSNM, site-specific nutrient management. doi:10.1371/journal.pbio.1001124.t003

.

PLoS Biology | www.plosbiology.org 3 August 2011 | Volume 9 | Issue 8 | e1001124

The Value and Consumption of N Fertilizers Are Both Rising

The global value of N fertilizers has

increased from US$32B annually in 1987

to over US$80B annually, and even

conservative estimates project it to in-

crease to US$150B by 2030 (Table 1).

Overall global consumption has increased

18% over the past 20 years, due in most

countries to an increase in cereal produc-

tion [9]. The N balance within countries

and regions reflects the N input to output

ratio as surplus, neutral, or deficit. A

surplus N balance leads to NH3, N2O,

NO3 2

, and or NO pollution while a deficit

N balance leads to low soil fertility from

depleting soil nutrient pools, resulting in

poor crop yield [10]. While overall some

countries, such as the US, have become

fairly balanced in their N input to output,

with little increase in overall N fertilizer

consumption since 1975, there are still

major areas of cropland that are rated as

having high N balances, resulting in soils

highly susceptible to losses of N2O to the

atmosphere [11]. Other regions, such as

the European Union (EU), have had

significant fertilizer N consumption reduc-

tions [12]. The large reduction in N

Box 1. Reducing Fertilizer Applications

Rice: For China, it was suggested that a reduction in N fertilizer application of 30% to 60% could be implemented for wheat, maize, and rice while still maintaining current crop yields [18]. The authors argued that reductions in N fertilizer usage would cause no significant reduction in yields in the rice/wheat and wheat/maize double-cropping systems in eastern and northern China, respectively. This is because the current N fertilizer application rates are upwards of 600 kg N ha-1 and much of this N is lost from the crop-soil system by leaching into the aquatic environment and atmospheric emissions ([18] and references within).

Japanese rice farmers use less N fertilizer currently on their crops than in the past, with no loss in yield. In the early 1990s, a fall in rice prices induced rice farmers to decrease their N fertilizer application rates from 109 kg N ha

-1 in 1985 to 80 kg N ha

-1 in

1997, while still maintaining rice yields. This success was attributed to the reduction of excessive fertilizer application and the use of an N use efficient rice variety called Koshihikari, which maintains high yield under a lower N regime [30]. Currently in Japan, nitrogen use efficiency (NUE) of rice has increased over 30% from 1985 to recent years [31].

On a broader scale, it has been demonstrated [32] that there was no correlation between countries that had high levels of yields for rice and the NUE of that country. For example, Japan had high rice yields and high NUE, whereas China had high yields but low NUE. In a multinational field trial program (179 farm sites in seven countries) for intensive rice production organized by the International Rice Research Institute (IRRI), rice grain yield was increased by 7% by balanced fertilizer use, although less N was applied [33].

Maize: There have been many N fertilization studies conducted with maize in the US, and some selected examples are shared here (Table 3). One study found that both the currently recommended N application rate (168 kg ha-1) and the farmers’ use (197 kg ha-1) exceeded the profit maximizing level of N by a minimum of 35% [34]. Minnesota farmers were able to reduce nitrogen use in corn by 21% without any reduction in crop yield [35]. Based on US Department of Agriculture statistics for US maize yield and fertilizer N used for corn production, from 1980 to 2000 US maize yields increased by 35% without significant increases in N fertilization levels [36]. A three-year Michigan corn study using different fertilizers, different fertilizer management strategies, and nine N fertilizer application rates (from 0 to 292 kg N ha-1) showed that using 101 kg N ha-1 maximized grain yield while minimizing N2O emissions, whereas using 134 kg N ha

-1 or more increased N2O emissions significantly [37]. These authors

concluded that N2O emissions could be reduced, without a yield penalty, by reducing N fertilizer inputs to a level that just satisfies the crops N requirement. A study conducted from 2007 to 2008 in Michigan at multiple commercial corn farms examining N2O response to six different N fertilizer rates (0-225 kg N ha

-1 ) showed that high rates of N fertilization led to (on

average) nonlinear increasing rates of N2O loss without economic yield gains [38]. When old versus modern maize hybrids were examined, modern hybrids had an optimal N application rate that was 18% less than older hybrids (160 kg ha-1 versus 195 kg ha-1), despite the fact that the modern varieties also had significant improvements in yield, in the range of 20% [39]. The research and education/extension programs of many of the land grant universities have been effective at reducing excess applications of N fertilizers; however, even The Economist was quick to point out that ‘‘Western countries have complacently cut back on the work done in universities and international institutions. It was a huge mistake. Basic farm research helps the whole world—and is a bargain’’ [40]. However, there have been studies to suggest that farmers applying BNMPs or new fertilizer technologies can reduce their N fertilizer application with no loss in yield [23,38]. A seven site-year study conducted on corn farms in Ontario, Canada, determined the effects of N fertilizer rate and timing on yield and N2O emissions [41]. The authors determined that although there was a slight increase in yield when fertilizer rate increased from 90 to 150 kg N ha-1, cumulative N2O emissions also doubled.

Wheat: There have been a number of studies that have demonstrated that modern wheat varieties have improved NUE (Table 3). Modern UK wheat varieties have shown a 14.6% to 18% increase in NUE, depending on the N conditions [42], while modern Spanish wheat varieties had a 24% to 29% increase in NUE (as measured by PFPN; [43]). A number of other UK wheat varieties have been evaluated and significant differences were determined in total N uptake and grain N uptake efficiency, depending on the N application rate [44]. These differences in NUE were primarily determined by greater yield, not increased concentrations of N in the plant material.

Barley: A number of studies have demonstrated that modern barley varieties have improved NUE (Table 3). Modern UK barley varieties, under optimally applied N conditions, had a 27% increase in NUE [41]. Also, modern Argentinean barley varieties had a 24% to 29% increase in NUE (as measured by PFPN) over older varieties [45]. Eight years of data for different varieties of spring barley grown in Canada were analyzed and the best performing varieties had a 7% to 17% improvement in NUE over the mean for all varieties [46].

.

PLoS Biology | www.plosbiology.org 4 August 2011 | Volume 9 | Issue 8 | e1001124

fertilizer consumption was achievable in

these countries because of an initial N

balance surplus that polluted the water

quality to an unacceptable level up to 1987

([12], Table 1). The EU successfully

implemented nutrient reduction programs

by developing best nutrient management

practices (BNMPs; [13])—such as coordi-

nating fertilizer requirements and applica-

tion methods and rates to particular crops,

soils, and soil water status—that have

improved the quality of ground water,

rivers, and lakes [14]. China is an example

of a region with high N balance surpluses

and an N fertilizer consumption rate that

is still on the rise. There are other regions

in the world that display N balance

deficits, for instance the countries of sub-

Saharan Africa, which have chronically

nutrient-poor soils and under-use N fertil-

izers [3].

Given the tremendous costs associated

with N fertilizer over-application, it’s

helpful to consider why the EU has

managed an overall reduction in N

fertilizer while countries such as China

have increased their use, how N fertilizer

usage could be reduced without compro-

mising crop yields, and what the economic

and environmental benefits of directed

nutrient management strategies might be.

Why Has There Been an Overall Decrease in N Fertilizer Application in Some Countries and Not in Others?

Within the EU, there has been a 56%

decrease in total fertilizer use between

1987 and 2007, including a significant

decrease in N application per hectare

(Table 1). In Denmark, for example,

producers have decreased the applied

nitrogen by 52% since 1985, resulting in

a 47% reduction in ammonia emissions

[14]. How was this achieved? Danish

agriculture was forced to employ sustain-

able agricultural methods after the adop-

tion of the Nitrate Directive in 1987

[15,16], which mandated the use of

BNMPs to reduce nitrate levels in drinking

water. After evaluating the most appropri-

ate BNMPs for specific crops, soils, and

different cropping systems and using

nutrient budgeting models (including or-

ganic N sources), Danish regulatory bodies

identified improved agronomic practices

(such as restricting fall N fertilizer appli-

cations, which are often leached as toxic

emissions over winter). From this research,

the government enacted legislation outlin-

ing specific N inputs and management

practices for each crop [14]. EU producers

are now required to provide detailed N

farm budgets before they can receive

Common Agricultural Policy (CAP) subsi-

dy payments [17].

Recent reports on Chinese agricultural

methods, in contrast, indicate that N

fertilizer use is much higher than required

for optimal yield, in some cases up to

600 kg N ha 21

[18]. The government

encouraged producers to use more fertil-

izer to attain higher yields and support

China’s domestic food security. However,

recent estimates of fertilizer usage in

China suggest that a reduction of 30% to

50% in applied fertilizer would not

necessarily reduce yields [18]. Assuming

a conservative reduction of 10% below

current usage, by 2020 China could

reduce its fertilizer use by 11.5 MMt per

year, compared to the predicted increase

in N application. This would result in

savings to Chinese producers of US$11.3B

annually (Table 2).

Reducing N Fertilizer Application without Reducing Yield

In the US, the United Kingdom, and

other countries, rice (Oryza sativa), maize

(Zea mays), wheat (Triticum aestivum), and

barley (Hordeum vulgare) have been grown

experimentally to determine their N re-

sponse to increasing fertilizer applications

(commonly expressed as an N response

curve; Table 3). These long-term studies

demonstrate that implementing BNMPs

can allow for a reduction in N fertilizer

application with no loss to yield, even in N

balanced systems. Also, for those develop-

ing countries that need to increase their N

fertilization rates, there is still a require-

ment to implement local specific manage-

ment strategies to increase yield and

reduce future excessive application rates

(Table 3).

Many field studies have been done in

various regions of the world, analyzing the

optimum BNMPs for the specific region,

including fertilizer rate, for a variety of

crops. All of these studies indicate that

reductions in fertilizer usage, in those

situations where it is being applied in

excess, can occur without any loss in yield

(see Box 1).

Economic and Environmental Benefits of Using Directed Nutrient Management Strategies

The economical optimal N rate

(EONR) is the rate of fertilizer that allows

for the maximum economic yield [19,20].

After the fertilizer price has been included,

a lower N fertilization rate than the

maximum yield rate should be applied.

What is now needed is a way to measure

the environmental and economic optimal

N rate (EEONR). This N rate takes into

account the N fertilizer price plus the cost

of the N lost to the environment. The

environmentally optimal N application

rate for maize was recently calculated,

suggesting that a rate of 25 kg ha 21

less

than the economic optimal N application

rate would reduce GHG emissions [21].

The Iowa State University Agronomy

Extension in 2004 recommended another

approach, the maximum return to N

(MRTN), using a range of economical N

inputs for US Midwest corn farmers that

take into account both N fertilizer prices

and corn prices [11]. Although this

approach does not directly take into

account environmental costs, it does

suggest a range of fertilizer rates, on

average, 185 kg N ha 21

(the high profit-

able N rate) to 158 kg N ha 21

(the low

profitable N rate) that are both below the

well-used and recommended yield goal N

Table 4. N losses to the environment and the calculated economic value of these costs for the US.

N Component Average (%) Range (%) Environmental Costs (US $B)

Plant product 40 30–50 NA

Tier 1 N2O-N emission factor 1 0.003–0.03 1.01B a

Leaching and runoff (Nitrate) 20 15–28 3.6B

N2O from volatized ammonia 20 15–25 0.47B b

Lost or denitrified 19 15–83 ND

Total 100 — 5.1B (44%)

Total N applied in the US in 2007 was 14.5 MMt at a value of US$11.5B. a 14.5MMt x 0.016(28+16 g mol21 / 28 g mol21 ) 6 2966$15/t = US$1.01B.

b(14.5 MMt N fertilizer US) / (83 MMt N fertilizer globally) 6(0.6 Tg N2O formed from ammonia volatilization) = 0.11 Tg N2O volatized ammonia in the US per year. 0.11 MMt N2O62966US$15/t = US$0.47B.

doi:10.1371/journal.pbio.1001124.t004

.

PLoS Biology | www.plosbiology.org 5 August 2011 | Volume 9 | Issue 8 | e1001124

rate of 250 kg N ha 21

, or more [11]. This

reduction in N fertilizer rate also reduced

N pollution of the ecosystem. Many

studies conducted in the US, especially

through the corn-belt region, show that

loss of N to crops can be reduced by

reduced N fertilizer application, manage-

ment practices, and type of fertilizer used

[22,23]. Nutrient management strategies

take into consideration not only N fertil-

izer application rate, but also factors

including type of tillage, type of N

fertilizer, and rotation with N fixing crops.

N fertilizer is needed to maintain or

increase crop yields; however, depending

on the tillage system and crop rotation

used, a high N application rate can

decrease farmer profits and increase N2O

emissions [23]. For example, corn farmers

in Colorado using a conventional tillage

and continuous corn (CT-CC) manage-

ment system can reduce both GWP and

increase net profits by reducing N fertilizer

application. If those same farmers

switched to a no-till corn-bean rotation

system, they could further reduce GWP

and increase profits but at a higher N

fertilizer rate than for CT-CC [23].

The type of N fertilizer applied can

directly affect N2O emissions as well.

Box 2. The Environmental Cost of Excess N Applications

Global atmospheric N2O concentrations have increased from the pre-industrial level of 270 ppb to 319 ppb in 2005, with agriculture (fertilizer use and animal production) as the primary source of this added N2O. N2O can remain in the atmosphere for approximately 114 years [47]. The FAO has predicted that by 2030 global N2O emissions from fertilizer and manure application will increase by 35% to 60% [38]. For the loss of N by emission of N2O via denitrification, we used the Intergovernmental Panel on Climate Change [47] linear Tier 1 N2O default emission factor of a 1% loss of applied N as N2O-N (1 kg of N2O-N emitted per 100 kg of applied N) which takes into consideration N2O-N emissions from N applied as mineral and organic fertilizers, crop residues and N mineralized from soil due to loss of soil carbon [47]. It should be noted, however, that N2O emissions can vary due to not only N fertilizer rate, but also soil type (texture, drainage, pH), soil organic carbon levels, climate, type of N fertilizer applied, method of fertilizer placement, and crop type grown [47,48]. Several studies conducted in the US and Canada have shown that N2O-N emission rates can be nonlinear, especially at higher N fertilizer rates, showing that higher N fertilizer rates can produce exponential N2O emissions [11,38,41]. Since this 1% N2O-N emission factor is an estimate, it may under-represent the actual N2O emission rate when the N fertilizer rate exceeds the crop or soil uptake ability [22]. Globally in 2005, N fertilizer use was approximately 93 MMt and caused an estimated emission of 1.46 MMt of N2O, equal to 433 MMt of carbon dioxide equivalents (CO2e) [48]. In 2007, in the US, 14.5 MMt of N were applied to crops [9], representing 0.228 MMt of N2O emissions, having the GWP of 67.4 MMt of CO2e. Therefore, the partial environmental cost of soil N2O emissions can be estimated based on the CO2 equivalency. Carbon dioxide credits are traded as commodities on the European and New Zealand CO2 exchanges, so they have a monetary value. When the value for CO2 is taken as US$15/ton, the N2O emissions in the US equates to a value of US$1.01B annually. Although N is also lost as NO2 and N2 (20% of applied N may be lost as N2; [49]) via nitrification and denitrification, there is no directly measurable cost associated with these types of N loss, so we did not include these in our partial estimates of environmental costs. As well, N2 does not have a negative environmental impact on the ecosystem.

One measure to determine the economic cost of excess nitrate from runoff and leaching would be to look at the economic and social impact excess N has against specific industries. As an example, about 8% of the N applied in the US corn-belt is being directly exported into the Gulf of Mexico via the Mississippi River [50]. This lost N has both a direct economic cost to the agricultural producers, but also has an indirect negative impact on other economic activities. In the Gulf of Mexico, commercial and recreational fisheries currently generate US$2.8B annually. However, one half of the shellfish and many oyster beds have either been permanently closed or declared indefinitely off-limits by health officials as a result of N pollution [51]. Therefore, we estimated the cost to the Gulf marine economy to be US$1.4B annually. An analysis of the economic cost of eutrophication of US freshwaters as it pertains to loss of recreational activities, property value, threatened and endangered species recovery efforts, and drinking water was recently completed [52]. Dodds et al. [52] provide a conservative estimate of the eutrophication cost to be US$2.2B annually for the US fresh waterways. Therefore, in total, a conservative cost estimate for excess runoff and leaching in the US is US$3.6B.

Losses of ammonia from N fertilizer application can be as high as 50% to 80%, depending on climate, type of fertilizer used, application method, and soil type [53]. Livestock manures and urea fertilizers tend to volatize the most ammonia globally at 23% and 21%, respectively [53]. Ammonia is not considered to have a direct GWP, so a direct cost of ammonia volatization is difficult to calculate. However, ammonia emissions affect air, water, and land quality, and can lead to ‘‘acid rain,’’ which causes marine and soil ecosystems to become acidic and in turn contributes to aquatic eutrophication and soil acidification [49]. High levels of ammonia and ammonium can reduce plant diversity, increase plant predation by insects, and cause serious human diseases, including cardiovascular and lung diseases and asthma [53]. Ammonia has a short life span in the atmosphere and is either dry deposited locally to the site of emission or converted in the atmosphere to ammonium (NH4

+), nitric oxides (NOx), and N2O. Ammonium can accumulate in clouds and be wet deposited in regions distant from the site of emission. Globally, synthetic fertilizers and agricultural crops account for 12% of total ammonia emissions [54]. Of the 83 MMt of N fertilizer used globally in 1996, an estimated 0.6 Tg of N2O was formed from atmospheric ammonia oxidation. Assuming similar losses in the US, 0.11 Tg of N2O was formed in 2007, with an indirect GWP cost of US$0.47B.

We determined the environmental costs from excess N to conservatively be 44% of the cost of the total N applied in the US. We then used this value in Table 2 to model the environmental costs associated with excess applied N for the world, the US, China, and India. While these gross cost estimates may not be accurate for any one crop, they provide a starting point for discussion. We fully recognize the challenges of accurately estimating site-specific N losses. However, the important goal is to identify the costs associated with the various types of N pollutants. These cost estimates can then be used to develop economic tools to ensure that the environmental costs are integrated into BNMPs.

.

PLoS Biology | www.plosbiology.org 6 August 2011 | Volume 9 | Issue 8 | e1001124

Research conducted in Colorado for two

years on N2O emission rates from irrigat-

ed no-till-corn grown with enhanced-

efficiency N fertilizers versus conventional

dry urea and liquid urea-ammonium

nitrate showed that the enhanced-efficien-

cy N fertilizers reduced N2O-N emissions

while maintaining yield [24]. Yields of

Minnesota potatoes were maintained

while reducing N2O emission by using

single, pre-plant applications of polymer-

coated urea for N fertilizer compared to

multiple split applications of conventional

uncoated urea [25]. As well as maintaining

yields with fewer N2O emissions, the N

fertilizer costs were reduced due to the

need for only a single application versus

multiple applications with conventional

urea.

N fertilizer (organic and inorganic) that

is not taken up by crop plants can be lost

to the environment through nitrification/

denitrification of ammonium/nitrate (re-

spectively) by soil microbes. N runoff and

leaching of nitrate into waterways (aqui-

fers, rivers, lakes, and oceans) and ammo-

nia volatization into the atmosphere can

also occur. While we recognize that losses

vary dramatically, depending on multiple

variables, we made a number of simple

assumptions to model these N losses from

excess N fertilizer applications and calcu-

late their economic costs to the environ-

ment. For most cereal crops, only 30% to

50% of applied N is actually taken up by

the plant [26,27]. Therefore, we assumed

that plants take up approximately 40% of

the available N with the remaining 60% as

surplus N. The fate of the surplus N can

include becoming an environmental pol-

lutant (Table 4), or held in soil as organic

or inorganic N, depending on the soil and

N type.

We attempted to determine the envi-

ronmental and associated economic costs

of N applications, using the US as an

example (see Box 2). The choice of the US

was based on the fact that there are better

data available. Using both fertilizer use

and price projections, we evaluated the

cost savings associated with reducing N

budgets such that they matched the

appropriate regional fertilizer recommen-

dations (Table 2). All countries analyzed in

Table 2 were assigned a neutral, or

reduction in N fertilizer use (5% to 20%),

based on analysis of their overuse of

fertilizers in the selected literature we have

cited (Table 3). While this analysis includ-

ed only four major regions/countries,

these collectively account for 74% of

global fertilizer use [9]. Based on this

analysis, savings of US$19.8B per year and

US$56B per year are attainable by 2020

and 2030 respectively, assuming no

change in the area of farmed land.

Several Simple Proposals to Reduce N fertilizer Use

It is clear from many studies that when

N application rates are in balance, N losses

via N2O emissions and leached nitrate are

reduced to a minimum, depending on the

cropping system [17,28]. Although dry

land cereal production in Canada is

usually based on a single, pre-planting

application of N fertilizer and mobilization

of the applied N is by rain-fed moisture,

many cropping systems allow revised

application rates, which, along with more

careful monitoring of the 4Rs (right

source, right time, right place, right rate),

can result in significant reductions of N

losses that harm the environment. Clearly,

by using BNMPs, the producer benefits

from reduced costs while everyone benefits

from an improved environment.

In order to successfully optimize the use

of N fertilizers (both agronomically and

environmentally), we propose several sim-

ple approaches. First, fertilizer use require-

ments need to be reassessed in virtually all

agricultural systems, from an economic

and environmental perspective. Second,

economic and environmental models need

to be integrated and be made user-

friendly, particularly in those developed

and developing countries where excessive

N use occurs. Third, countries need to

ensure that government programs do not

discriminate against producers who volun-

tarily choose to use less fertilizer. For

example, crop insurance often requires the

farmer to apply fertilizers at the recom-

mended (but potentially out-dated) rate,

otherwise they will not be compensated for

potential crop losses. Fourth, we need to

find economic tools to better inform and

drive changes in N application rates. It is

easy to say that reducing rates will help

reduce N2O emissions, but the producer

does not benefit economically from that,

unless there is some form of payment for

reducing N applications. This is effectively

providing a global ecological service.

Some countries, such as Austria and

Finland [29], have begun to implement

‘‘green taxes’’ (i.e., taxes on fertilizers and

agrichemicals). However, at a minimum,

we need to eliminate ‘‘negative green

incentives’’, which often provide direct

subsidies to farmers to use fertilizers.

Regardless of the tools used to promote

change (legislative, economic), education

programs need to be put in place imme-

diately to promote the environmental and

economic benefits of the optimal use of N

fertilizer.

In Conclusion

Through a combination of the 4R

BNMPs and advances in fertilizer tech-

nology and plant genetics, it may be

possible to reduce global N application

rates by 20% by 2050, saving US$150B

annually, compared to business as usual.

Unlike many of the challenges faced by

agriculture, reducing excess nutrient ap-

plications (as demonstrated by the EU) is

within our ability. Finally, farmers, scien-

tists, and economists need to communicate

more efficiently to promote the use of the

EEONR and BNMPs while providing

scientific data and leadership to address

this issue.

Acknowledgments

The authors thank Rebecka Carroll, Jayne

D’Entremont, and Juan Wang for their help,

comments, and discussions, and an anonymous

reviewer for valuable input and insights.

References

1. Hardin G (1968) The tragedy of the commons. Science 162: 1243–1248.

2. Brown, LR (2011) World on the edge. How to

prevent environmental and economic co- llapse. New York: W.W. Norton & Company.

240 p.

3. Vitousek PM, Naylor R, Crews T, David MB,

Drinkwater LE, et al. (2009) Nutrient imbalances

in agricultural development. Science 324: 1519–1520.

4. Powlson DS, Addiscott TM, Benjamin N, Cassman KG, de Koky TM, et al. (2006) When

does nitrate become a risk for humans? J Environ.

Qual 37: 291–295.

5. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, et al. (2008) Transformation

of the nitrogen cycle: Recent trends, questions,

and potential solutions. Science 320: 889– 892.

6. U.S. Environmental Protection Agency (2007) Hypoxia in the Northern Gulf of Mexico: an

update by the EPA Science Advisory Board.

EPA-SAB-08-003. Washington (D.C.): U.S. En- vironmental Protection Agency.

7. U.S. Environmental Protection Agency (2010) Inventory of U.S. greenhouse gas emissions and

sinks: 1990-2008. 15 April 2010, EPA 430-R-10-

006. Washington (D.C.): U.S. Environmental

Protection Agency. Available: http://epa.gov/

climatechange/emissions/usgginv_archive.html.

Accessed 20 July 2011.

8. Denman KL, Brasseur G, Chidthaisong A,

Ciais P, Cox PM, et al. (2007) Couplings

between changes in the climate system and

biogeochemistry. In: Solomon S, Qin D,

Manning M, Chen Z, Marquis M, et al.

(2007) Climate change 2007: the physical

science basis. Contribution of Working Group

I to the Fourth Assessment Report of the

Intergovernmental Panel on Climate Change.

Cambridge: Cambridge University Press. pp

499–587.

.

PLoS Biology | www.plosbiology.org 7 August 2011 | Volume 9 | Issue 8 | e1001124

9. Food and Agriculture Organization (2010) FAO-

STAT. Available: http://faostat.fao.org/. Data retrieved 1 June 2010.

10. Bouwman AF, van Drecht G, van der Hoek KW

(2005) Surface N balance and reactive N loss to

the environment from global intensive agricultur- al production systems for the period 1970-2030.

Science in China 48: 1–13.

11. Millar N, Robertson GP, Grace PR, Gehl RJ,

Hoben JP (2010) Nitrogen fertilizer management for nitrous oxide (N2O) mitigation in intensive

corn (Maize) production: an emissions reduction protocol for US Midwest agriculture. Mitig Adapt

Strateg Glob Change 15: 185–204.

12. Andersen JM, Boutrup S, van der Bijl L,

Svendsen LM, Bøgestrand J, et al. (2006) Aquatic and terrestrial environment 2004. State and

trends - technical summary. NERI Technical

Report No. 579. Copenhagen: National Environ- mental Research Institute, Ministry of the Envi-

ronment, Denmark. Available: http://www2. dmu.dk/1_viden/2_Publikationer/3_fagrappor

ter/rapporter/FR579.pdf. Accessed 15 July

2011.

13. International Plant Nutrition Institute (2009) The global ‘‘4R’’ nutrient stewardship framework:

developing fertilizer best management practices

for delivering economic, social and environmental benefits. Available: http://www.ipni.net/4r.

Accessed 15 July 2011.

14. Olesen JE, Sorensen P, Thomsen IK, Eriksen J,

Thomsen AG, et al. (2004) Integrated nitrogen input systems in Denmark. In: Mosier AR, Syers

JK, Freney JR, editors. Agriculture and the nitrogen cycle. Assessing the impacts of fertilizer

use on food production and the environment. Washington (D.C.): SCOPE 65, Island Press.

Chapter 9.

15. European Commission (2010) The EU Nitrates

Directive. Available: http://ec.europa.eu/environ ment/water/water-nitrates/index_en.html. Ac-

cessed 15 July 2011.

16. Frederiksen P, Maenpaa M, eds (2007) Analysing

and synthesising European legislation in relation to water. A Watersketch Report under WP1.

NERI Technical Report No. 603. Copenhagen:

National Environmental Research Institute, Min- istry of the Environment, Denmark. Available:

http://www2.dmu.dk/Pub/FR603.pdf. Accessed 15 July 2011.

17. Goulding K, Jarvis S, Whitmore A (2008) Optimizing nutrient management for farm sys-

tems. Philos. Trans R Soc London Ser B 363: 667–680.

18. Ju X-T, Xing G-X, Chen X-P, Zhang S-L, Zhang L-J, et al. (2009) Reducing environmental

risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci

USA 106: 3041–3046.

19. Scharf PC, Kitchen NR, Sudduth KA, Davis JG,

Hubbard VC, et al. (2005) Field-scale variability in optimal N fertilizer rate for corn. Agron J 97:

452–461.

20. Scharf PC, Kitchen NR, Sudduth KA, Davis JG

(2006) Spatially variable corn yield is a weak predictor of optimal nitrogen rate. Soil

Sci Soc Am J 70: 2154–2160.

21. Kim S, Dale BE (2008) Effects of nitrogen fertilizer

application on greenhouse gas emissions and economics of corn production. Environ Sci Technol

42: 6028–6033.

22. Snyder CS, Bruulsema TW, Jensen TL, Fixen PE

(2009) Review of greenhouse gas emissions from crop production systems and fertilizer manage-

ment effects. Agric. Ecosyst. Environ 133:

247–266.

23. Archer DW, Halvorson AD (2010) Greenhouse Gas Mitigation Economics for Irrigated Cropping

Systems in Northeastern Colorado. Soil Sci. Soc.

Am. J. 74: 446–452.

24. Halvorson AD, Del Grosso SJ, Alluvione F (2010) Nitrogen source effects on nitrous oxide emissions

from irrigated no-till corn. J Environ Qual 39:

1554–1562.

25. Hyatt CR, Venterea RT, Rosen CJ, McNearney M,

Wilson ML, et al. (2010) Polymer-coated urea

maintains potato yields and reduces nitrous oxide

emissions in a Minnesota loamy sand. Soil Sci.

Soc Am J 74: 419–428.

26. Dobermann A, Cassman KG (2002) Plant

nutrient management for enhanced productivity

in intensive grain production systems of the

United States and Asia. Plant Soil 247: 153–175.

27. Kitchen NR, Goulding KWT, Shanahan, JF

(2008) Proven practices and innovative technolo-

gies for on-farm crop nitrogen management. In:

Follett RF, Hatfield JL, eds. Nitrogen in the

environment: sources, problems, and manage-

ment. Amsterdam: Elsevier. pp 483–517.

28. Van Groenigen JW, Velthof GL, Oenema O,

Van Groenigen KJ, Van Kessel C (2010)

Towards an agronomic assessment of N2O

emissions: a case study for arable crops. Europ.

J Soil Sci 61: 903–913.

29. Buttel FH (2003) Internalizing the societal costs of

agricultural production. Plant Physiol 133:

1656–1665.

30. Mishima S, Taniguchi S, Komada M (2006)

Recent trends in nitrogen and phosphate use and

balance on Japanese farmland. Soil Sci. Plant

Nutr 52: 556–563.

31. Mishima S (2001) Recent trends of nitrogen flow

associated with agricultural production in Japan.

Soil Sci. Plant Nutr. 47: 157–166.

32. Roy RN, Misra RV (2002) Economic and

environmental impact of improved nitrogen

management in Asian rice-farming systems. In:

Sustainable rice production for food security.

Proceedings of the 20th Session of the Interna-

tional Rice Commission. Bangkok, Thailand, 23–

26 July 2002. Available: http://www.fao.org:80/

docrep/006/y4751e/y4751e00.HTM. Accessed

15 July 2011.

33. Dobermann A, Witt-C, Dawe D, Abdulrachman-

S, Gines HC, et al. (2002) Site-specific nutrient

management for intensive rice cropping systems

in Asia. Field Crop Res 74: 37–66.

34. Yadav SN, Peterson W, Easter KW (1997) Do

farmers overuse nitrogen fertilizer to the detri-

ment of the environment? Environ and Res Ec 9:

323–340.

35. Wall D, McGuire SA, Magner JA (1989) Water

quality monitoring and assessment in the Garvin

Brook Rural Clean Water Project Area. St. Paul:

Division of Water Quality, Minnesota Pollution

Control Agency.

36. Cassman KG, Dobermann AR, Walters DT

(2002) Agroecosystems, nitrogen-use efficiency,

and nitrogen management. Ambio 31: 132–140.

37. McSwiney, CP, Robertson, GP (2005) Nonlinear

response of N2O flux to incremental fertilizer

addition in a continuous maize (Zea mays L.)

cropping system. Global Change Biol 11:

1712–1719.

38. Hoben JP, Gehl RJ, Millar N, Grace PR,

Robertson GP (2011) Nonlinear nitrous oxide

(N2O) response to nitrogen fertilizer in on-farm

corn crops of the US Midwest. Global Change

Biol 17: 1140–1152.

39. Moose S, Below FE (2009) Biotechnology ap-

proaches to improving maize nitrogen use

efficiency. In: Kriz AL, Larkins BA, eds. Molec-

ular genetic approaches to maize improvement,

biotechnology in agriculture and forestry. Berlin

Heidelberg: Springer-Verlag. 63 p.

40. The Economist (24 February 2011) The future of

food. The Economist. Available: http://www.

economist.com/research/articlesBySubject/Printer

Friendly.cfm?story_id=18229412. Accessed 20

July 2011.

41. Ma B, Wu L, Tremblay Y, Deen N, Morrison W,

McLaughlin MJ, et al. (2010) Nitrous oxide fluxes

from corn fields: on-farm assessment of the

amount and timing of nitrogen fertilizer. Global

Change Biol 16: 156–170.

42. Sylvester-Bradley R, Kindred DR (2009) Analys-

ing nitrogen responses of cereals to prioritize

routes to the improvement of nitrogen use

efficiency. J Exp Bot 60: 1939–1951.

43. Acreche MM, Slafer GA (2009) Variation of grain

nitrogen content in relation with grain yield in old

and modern Spanish wheats grown under a wide

range of agronomic conditions in a Mediterra-

nean region. Journal Agri Sci 147: 657–667.

44. Barraclough PB, Howarth JR, Jones J, Lopez-

Bellido R, Parmar S, et al. (2010) Nitrogen

efficiency of wheat: genotypic and environmental

variation and prospects for improvement. Eur.

J Agron 33: 1–11.

45. Abeledo LG, Calderini DF, Slafer GA (2008)

Nitrogen economy in old and modern malting

barleys. Field Crop Res 106: 171–178.

46. Anbessa Y, Juskiw P, Good A, Nyachiro J, Helm J

(2009) Genetic variability in nitrogen use efficien-

cy of spring barley. Crop Sci 49: 1259–1269.

47. Intergovernmental Panel on Climate Change

(2006) N2O emissions from managed soils, and

CO2 emissions from lime and urea application.

Chapter 11. In: Intergovernmental Panel on

Climate Change guidelines for national green-

house gas inventories. Volume 4: Agriculture,

forestry and other land use. Available: http://

w ww . i p c c -n g g i p . i g e s . o r . j p / p u b l i c/ 20 0 6 g l/

pdf/4_Volume4/V4_11_Ch11_N2O&CO2.

pdf. Accessed 15 July 2011.

48. Snyder CS, Bruulsema TW, Casarin V, Chen F,

Jaramillo R, et al. (2010) Global crop intensifica-

tion lessens greenhouse gas emissions. Better

Crops 94: 16–17.

49. Mosier AR, Syers JK, Freney JR, eds (2004)

Agriculture and the nitrogen cycle. Assessing the

impacts of fertilizer use on food production and

the environment. Washington (D.C.): SCOPE 65,

Island Press. 291 p.

50. Battaglin WA, Kendall C, Chang CCY, Silva SR,

Campbell DH (2001) Chemical and isotopic

evidence of nitrogen transformation in the Mis-

sissippi River, 1997–98. Hydrol Process 15:

1285–1300.

51. Mitsch WJ, Day Jr. JW, Gilliam W, Groffman PM,

Hey DL, et al. (2001) Reducing nitrogen loading to

the Gulf of Mexico from the Mississippi River

basin: strategies to counter a persistent ecological

problem. Bioscience 51: 373–388.

52. Dodds WK, Bouska WW, Eitzmann JL, Pilger TJ,

Pitts KL, et al. (2009) Eutrophication of u.s.

freshwaters: analysis of potential economic dam-

ages. Environ. Sci Technol 43: 12–19.

53. Dragosits U, Dore AJ, Sheppard LJ, Vieno M,

Tang YS, et al. (2008) Sources, dispersion and

fate of atmospheric ammonia. In: Follett RF,

Hatfield JL, eds. Nitrogen in the environment:

sources, problems, and management. Amster-

dam: Elsevier Inc. pp 333–393.

54. Aneja VP, Blunden J, James K, Schlesinger WH,

Knighton R, et al. (2008) Ammonia assessment

from agriculture: U.S. status and needs.

J Environ Qual 37: 515–520.

55. Frink CR, Waggoner P, Ausubel JH (1999)

Nitrogen fertilizer: retrospect and prospect. Proc.

Natl Acad Sci U S A 96: 1175–1180.

56. Daberkow S, Poulisse J, Vroomen H (2000)

Fertilizer requirements in 2015 and 2030. ISBN

92-5-104450-3. Rome: FAO.

57. Tilman D, Fargione J, Wolff B, D’Antonio C,

Dobson A, et al. (2001) Forecasting agriculturally

driven global environmental change. Science 292:

281–284.

58. Galloway JN, Dentener FJ, Capone DG,

Boyer EW, Howarth RW, et al. (2004) Nitrogen

cycles: past, present, and future. Biogeochemistry

70: 153–226.

59. Matson PA, Naylor R, Ortiz-Monasterio I (1998)

Integration of environmental, agronomic and

economic aspects of fertilizer management. Sci-

ence 280: 112–115.

60. Schmidt JP, DeJoia AJ, Ferguson RB, Taylor RK,

Young RK, et al. (2002) Corn yield response to

nitrogen at multiple in-field locations. Agron J 94:

798–806.

.

PLoS Biology | www.plosbiology.org 8 August 2011 | Volume 9 | Issue 8 | e1001124

61. Dobermann A (2006) Nitrogen use efficiency in

cereal systems. In: Proceedings of the 13th

Australian Agronomy Conference; 10–14 Sep-

tember; Perth, Western Australia. Australian

Society of Agronomy. Available: http://www.

regional.org.au/au/asa/2006/plenary/soil/do-

bermannad.htm. Accessed 15 July 2011.

62. Cassman KG, Dobermann A, Walters DT,

Yang H (2003) Meeting cereal demand while

protecting natural resources and improving

environmental quality. Annu. Rev. Environ.

Resour 28: 315–358. 63. Wang GH, Dobermann A, Witt C, Sun QZ,

Fu RX (2001) Performance of site specific

nutrient management for irrigated rice in South- east China. Agron J 93: 869–878.

.

PLoS Biology | www.plosbiology.org 9 August 2011 | Volume 9 | Issue 8 | e1001124

Copyright of PLoS Biology is the property of Public Library of Science and its content may not be copied or

emailed to multiple sites or posted to a listserv without the copyright holder's express written permission.

However, users may print, download, or email articles for individual use.