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64
© Royal Swedish Academy of Sciences 2002 Ambio Vol. 31 No. 2, March 2002
http://www.ambio.kva.se
INTRODUCTION
The late-18th century–N discovered.
The late-19th century–natural N fixation discovered.
The late-20th century–anthropogenic N fixation exceeded natu-
ral terrestrial N fixation.
Nitrogen is the very stuff of life. It constitutes a major part of
the nucleic acids that determine the genetic character of all liv-
ing things and the enzyme proteins that drive the metabolic ma-
chinery of every living cell. Triple-bonded nitrogen gas (N
2
)
makes up nearly 80% of the total mass of the Earth’s atmosphere.
To most organisms, this huge reservoir of N is not biologically
available. Before N can be used by most plants, animals, insects,
and microorganisms, the triple bonds of N
2
molecules must be
broken and the resulting single-N atoms must be bonded chemi-
cally with one or more of 3 other essential nutrient elements –
oxygen and/or hydrogen through N-fixation processes and car-
bon through N-assimilation processes (1).
Breaking the triple bonds within the N
2
molecule is an energy-
requiring reaction. In nature, fixation of N
2
is accomplished
mainly by certain unique microorganisms that have developed
the special metabolic machinery necessary to produce biologi-
cally active reduced forms of nitrogen such as ammonia, amines,
and amino acids – the structural constituents of proteins and nu-
cleic acids (2). These specialized organisms include a few free-
living bacteria and blue-green algae, and also certain symbiotic
bacteria that have developed special metabolic relationships with
the roots of leguminous crop plants such as soybeans, clover,
and N-fixing trees such as alder. Oxidative fixation of gaseous
N
2
leads to production of reactive oxidized forms of N. Oxidative
fixation of N also takes place in nature, but only in high-tem-
perature natural processes such as lightning.
In the pre-human world, biological nitrogen fixation was the
dominant means by which new reactive nitrogen (Nr) (3) was
made available to living organisms. The total amount of Nr that
circulated naturally among various compartments of the atmos-
phere and the biosphere of the Earth was quite small. Thus, the
biodiversity and intricate webs of relationships found in nature
evolved as a result of intensive competition among many dif-
ferent life forms – most of them evolving under N-limited con-
ditions.
During the last 2 centuries, human involvement with N be-
gan with discovery of N as an element (late-18
th
century). This
led to the discovery of biological nitrogen fixation (late-19
th
cen-
tury), and eventually to the human dominance of the global rate
of N fixation (late-20
th
century). This paper presents an assess-
ment of the impact of humans on the biogeochemical cycle of
N due to the enhanced creation of reactive-N. Following a his-
torical overview, this paper discusses the changes in N-mobili-
zation rates due to human activities, the resultant changes in the
distribution fluxes to waters and the atmosphere, and an assess-
ment of the environmental consequences of these changes. The
paper concludes with an overview of regional differences in hu-
man alteration of the N cycle, casts an eye toward the future and
presents the case for developing a Total Nr Approach for man-
agement of N.
HISTORICAL CONTEXT
Two hundred years span the time from discovery of N as an el-
ement to the present time of human dominance in Nr creation.
Over that period, the global human population increased from
~ 0.85 billion to ~ 6.2 billion. This section presents significant
discoveries regarding N in the context of a growing human popu-
lation (Fig. 1). Unless otherwise noted, historical information is
taken from Smil (4).
Nitrogen was discovered in the late 18
th
century through the
work of several early chemists–Scheele (1742–1786, Sweden),
Rutherford (1749–1819, Scotland), Lavoisier (1743–1794,
France). It was formally named ‘nitrogene’, by the French sci-
entist, Chaptal (1756–1832). Nitrogen’s role in crop production
was not recognized until the mid-19
th
century, initially by
Boussingault (1802–1887) and then more thoroughly by von
Liebig (1803–1873), who developed the theory of nutrient limi-
tation in plant productivity. Near the end of the 19
th
century,
Hellriegel (1831–1895) and Wilfarth (1853–1904) discovered
that microbial communities could extract nonreactive N
2
from
the atmosphere and convert it into a useable form—biological
nitrogen fixation (BNF).
Less than 50 years after N was first identified as an essential
nutrient for all plants and animals it was also discovered that
the growing demand for food by increasing human populations
was exceeding known sources. In 1898, Sir William Crookes,
president of the British Association for the Advancement of Sci-
ence, stated: “All England and all civilized nations stand in
deadly peril of not having enough to eat” due to the increasing
demands for food and the lack of biologically available nitro-
Reactive Nitrogen and The World:
200 Years of Change
James N. Galloway and Ellis B. Cowling
This paper examines the impact of food and energy
production on the global N cycle by contrasting N flows in
the late-19
th
century with those of the late-20
th
century. We
have a good understanding of the amounts of reactive N
created by humans, and the primary points of loss to the
environment. However, we have a poor understanding of
nitrogen’s rate of accumulation in environmental reservoirs,
which is problematic because of the cascading effects of
accumulated N in the environment. The substantial region-
al variability in reactive nitrogen creation, its degree of dis-
tribution, and the likelihood of increased rates of reactive-
N formation (especially in Asia) in the future creates a
situation that calls for the development of a Total Reactive
Nitrogen Approach that will optimize food and energy
production and protect environmental systems.
Figure 1. Global population trends (36, 53) with key dates for the
discovery of N as an element in the periodic table and its role in
various biogeochemical processes. Also shown is an estimate of the
annual production of Nr by the Haber-Bosch process.
65Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
gen (5). This realization triggered a global search for natural de-
posits of reactive-N that could be used as fertilizer. At the end
of the 19
th
century and the beginning of the 20
th
century, the arid
islands of the Pacific and the deserts of South America yielded
guano and nitrate deposits which were mined for Nr to grow food
in Europe and elsewhere. But other sources were needed. A very
timely breakthrough occurred in 1913, invention of a chemical
process to convert atmospheric N
2
to NH
3
. The Haber-Bosch
process allowed, for the first time, an unlimited supply of nitro-
gen that could be used to grow food (and make explosives).
After the Haber-Bosch process was invented, the global hu-
man population started growing rapidly. While there are many
reasons for this, availability of food was an important factor.
Today, more than half of the food eaten by the world’s peoples
is produced using nitrogen fertilizer from the Haber-Bosch proc-
ess (4).
Energy production also creates Nr, although in contrast to food
production, it is produced by accident as a consequence of fos-
sil-fuel combustion. The sources of Nr in energy production are
twofold—conversion of atmospheric N
2
to NO
x
and conversion
of fossil organic N in the fuel to NO
x
. Both sources result in in-
creased Nr—one from creation of new Nr, and the other from
release of sequestered Nr (6). While there are records of coal
use in China dating from 500 BC, until the late-19
th
century, most
energy was produced from biofuels (e.g. wood). It wasn’t until
the beginning of the 20
th
century that fossil fuels exceeded
biomass fuels in supplying primary energy (7).
Nr CREATION: PAST AND PRESENT
This section presents the sources and amounts of Nr produced
by natural and anthropogenic processes in the past (1890) and
the present (1990). 1890 is an appropriate starting point for ex-
amination of the N cycle since there was limited Nr creation by
human activities. Although the global population was ~ 25% of
the current number, the world was primarily agrarian and pro-
duced only 2% of the energy and 10% of the grain produced to-
day. Most energy (75%) was provided by biomass fuels; coal
provided most of the rest (7). Petroleum and natural-gas produc-
tion was very limited and was of little consequence relative to
the global supply of energy and the creation of Nr as NO
x
through combustion. In total, fossil-fuel combustion created only
about 0.6 Tg N yr
–1
in 1890, through production of NO
x
(8).
Crop production was primarily sustained by recycling crop
residue and manure on the same land where food was raised.
Since the Haber-Bosch process was not yet invented, the only
new Nr created by human activities was by legume and rice cul-
tivation (the latter promotes Nr creation because rice cultivation
creates an anaerobic environment which enhances nitrogen fixa-
tion). While estimates are not available for 1890, Smil estimates
that in 1900 cultivation-induced Nr creation was on the order
of 15 Tg N yr
–1
(9, and pers. comm.). Additional Nr was mined
from guano (~ 0.02 Tg N yr
–1
) and nitrate deposits (~ 0.13 Tg
N yr
–1
) (10).
Thus in 1890, the total anthropogenic Nr creation rate was
~ 15 Tg N yr
–1
, almost entirely for food production. In contrast,
the natural rate of Nr creation was on the order of 300 Tg N
yr
–1
. Terrestrial ecosystems created ~ 100 Tg N yr
–1
(11) and ma-
rine ecosystems created ~ 140 Tg N yr
–1
(D. Capone, pers.
comm.). An additional ~ 5 Tg N yr
–1
was fixed by lightning (11).
On a relative basis for the globe, human activities created about
5% of the total Nr fixed and about 13% when only terrestrial
systems are considered.
One century later, the world’s population had increased by a
factor of ~ 3.5, from about 1.5 to about 5.3 billion, but the glo-
bal food and energy production increased about 7-fold (10) and
90-fold (7, 12), respectively. Just as was the case in 1890, in
1990 (and now) food production accounts for most of the new
Nr created. What changed most since 1890 was the magnitude
of Nr created by humans. Galloway et al. (11) estimated that in
1990 cultivation-induced Nr creation was ~ 40 Tg N yr
–1
. Smil
(9) estimated that in the mid-1990s it ranged from 25-41 TgN
yr
–1
, with a mean value of 33 Tg N yr
–1
, which we use in this
paper. The Haber-Bosch process, which did not exist in 1890,
created ~ 85 Tg N yr
–1
in 1990, mostly for fertilizer (~ 78 Tg N
yr
–1
) and the remainder in support of industrial activities such
as the manufacture of synthetic fibers, refrigerants, explosives,
rocket fuels, nitroparaffins, etc. (9, 12–14).
For energy production, during the period 1890 to 1990, much
of the world was transformed from a biofuel to a fossil-fuel
economy. The increase in energy production by fossil fuels re-
sulted in increased NO
x
emissions—from ~ 0.6 Tg N yr
–1
in 1890
to ~ 21 Tg N yr
–1
in 1990 (8, 15). By 1990 over 90% of energy
production resulted in the creation of new Nr, contrasting to 1890
where very little energy production caused Nr creation.
Thus, in 1990, Nr created by anthropogenic activities was
~ 140 Tg N yr
–1
, a ~ 9-fold increase over 1890, contrasted to a
~ 3.5-fold increase in global population. Coupled with the in-
crease in Nr creation by human activities, was a decrease in natu-
ral terrestrial N fixation because of conversion of natural
grasslands and forests to croplands, etc. from ~ 100 Tg N yr
–1
to ~ 89 Tg N yr
–1
(C. Cleveland, pers. comm.).
What is the fate of anthropogenic Nr? The immediate fate for
the 3 anthropogenic sources is clear—NO
x
from fossil-fuel com-
bustion is emitted directly into the atmosphere; RNH
2
from rice
and legume cultivation is incorporated into biomass; NH
3
from
the Haber-Bosch process is primarily converted into commer-
cial fertilizer which is applied to agroecosystems to produce
food. However, little of this fertilizer-N actually enters the hu-
man mouth. To put into context our later discussion of Nr dis-
persal through environmental reservoirs, it is useful to contrast
how much Nr the human body requires, relative to how much
Nr is produced by human beings via the Haber-Bosch process
for fertilizer.
THE HUMAN BODY
VS
THE HUMAN BEING:
NITROGEN AND FOOD
The human body requires ~ 2 kg N yr
–1
of protein to survive
(10). For thousands of years the collective human metabolic N
requirement was met by the goods and services provided by
unmanaged ecosystems—in essence using the nitrogen produced
by naturally occurring BNF. As populations increased and agri-
culture developed, natural sources of N had to be supplemented
with additional sources. Cultivation of rice was the first instance
of human-induced BNF through the construction of rice paddies
which, when anaerobic, create an environment of enhanced BNF.
Archeological evidence suggests that rice has been feeding hu-
mans for more than 8000 years (16, 17). Planting of legumes
was the second instance of human-induced BNF, with the first
substantiated citation of the soybean being in 1000 BC (18).
In contrast to those earliest times of anthropogenic BNF, the
1990 human population of ~ 5.3 billion created about ~ 110 Tg
N yr
–1
of Nr for food production, but needed only ~ 11 Tg (at 2
kg person
–1
yr
–1
). What happens to the ~ 100 Tg N yr
–1
that is
produced but not needed? Some is consumed as excess Nr, but
most is distributed to the environment without entering the hu-
man mouth; of course, all the Nr that enters the human mouth
is also eventually released to the environment.
There are several steps in the N cycle where leaks to the en-
vironment occur: between Haber-Bosch factory and field, be-
tween field and crop, between crop and harvest, between har-
vest and product, and lastly between product and mouth. We il-
lustrate the losses and the reasons by tracking the fate of 100 N
atoms formed into fertilizer by the Haber-Bosch process (Fig.
2a). These average estimates are derived from the analyses of
Bleken and Bakken (19), Mosier et al. (20), and Smil (4, 12, 21).
There is substantial variability in the following numbers but not
66
© Royal Swedish Academy of Sciences 2002 Ambio Vol. 31 No. 2, March 2002
http://www.ambio.kva.se
a.
b.
in the ultimate result—most of the Nr that is created for food
production does not enter the human mouth.
Factory to field: Of the 100 N atoms produced, 94 are applied
to the agricultural field as fertilizer. The remainder is lost to the
environment during fertilizer production, transport (railway,
pipeline, truck), storage at the factory, the distributor and the
farm (Fig. 2a).
Field to crop: Of the 94 atoms applied to the field, only about
half are taken up by the crop. The remainder is emitted to the
atmosphere (as NH
3
, NO, or N
2
O), or is lost to groundwater or
surface water as primarily nitrate.
Crop to harvest: Of the 47 N atoms incorporated into plant pro-
tein only 31 are in the harvested crop. The rest are lost from the
plant during its growth, or are not harvested (crop residue).
Harvest to food product: There are now 31 N atoms remaining.
If the harvested material is to be fed to humans, then the pro-
duction of a food product results in loss of 5 atoms of N due to
spoilage, product preparation, etc.
Product to mouth: Of the remaining 26 N atoms, 12 are lost due
to spoilage and waste. Thus, the efficiency of growing plant pro-
tein to feed to humans is about 14%. The remaining 86% of the
N is either recycled to agroecosystems or lost to the environ-
ment.
There is of course another use of the harvested crop, the pro-
duction of animal protein. Up to the third step above, the path-
way is the same. But we need to revisit the last two steps (Fig.
2b).
Harvest to feed product: There are now 31 N atoms remaining.
If the harvested crop is fed to animals which are then prepared
into a product, then 24 of the 31 N atoms are lost due to animal
metabolism and product preparation.
Product to mouth: Of the remaining 7 N atoms that are contained
in an animal protein product, 3 are lost due to spoilage and waste.
Thus, the efficiency of growing animal protein to feed to hu-
mans is about 4%. As above, the remaining 96% of the N is ei-
ther recycled to agroecosystems (e.g. manure) or lost to the en-
vironment.
cant alteration as a consequence of human action during the 100
years between 1890 and 1990.
In 1890, creation of Nr was dominated by natural processes
(Fig. 3a). The total anthropogenic Nr creation rate was ~ 15 Tg
N yr
–1
from legume/rice cultivation (actual year of estimate is
1900) and ~ 0.6 Tg N yr
–1
from fossil-fuel combustion. Natural
Nr production in terrestrial systems was ~ 100 Tg N yr
–1
, plus
an additional 5 Tg N yr
–1
fixed by lightning. There were limited
Nr transfers via atmospheric and hydrologic pathways relative
to the amount of Nr created by both natural and anthropogenic
processes. For terrestrial systems, of the ~ 100 Tg Nr yr
–1
cre-
ated, only about ~ 15 Tg N yr
–1
were emitted to the atmosphere
as either NH
3
or NO
x
. There was limited connection between ter-
restrial and marine ecosystems. Only about 5 Tg N yr
–1
of DIN
were transferred via rivers into coastal ecosystems in 1890, and
only about 17 Tg N yr
–1
were deposited to the ocean surface.
In 1990, by contrast, creation of Nr was dominated by human
activities (Fig. 3b). Natural terrestrial Nr creation was ~ 89 Tg
N yr
–1
, compared to cultivation-induced Nr creation of ~ 33 Tg
N yr
–1
, Haber-Bosch Nr creation of ~ 85 Tg N yr
–1
and fossil
Figure 2. The fate of fertilizer N produced by the Haber-Bosch process
from the factory to the mouth for (a) vegetarian diet, and (b)
carnivorous diet.
Figure 3. Global nitrogen budget for (a) 1890, and (b) 1990, Tg N yr
–1
. The
emissions to the ‘NO
y
box’ from the ‘coal’ reflect fossil-fuel combustion. Those
from the ‘vegetation’ include agricultural and natural soil emissions, and
combustion of biofuel, biomass (savannah and forests) and agricultural waste.
The emissions to the ‘NH
x
box’ from the ‘agricultural field’ include emissions
from agricultural land and combustion of biofuel, biomass (savannah and
forests) and agricultural waste. The NH
x
emissions from the ‘cow’ and ‘feedlot’
reflect emissions from animal waste. (For more details, see the section on
“Global N Cycle: Past and Present” this paper).
In summary, the human body needs about 2 kg
person
–1
yr
–1
, but human beings (collectively) create ~
20 kg person
–1
yr
–1
during food production processes.
While all of the Nr is distributed to the environment,
the Nr that does not enter the human mouth represents
an addition of a biogeochemically active element that
has both beneficial and detrimental consequences for
environmental systems.
THE GLOBAL N CYCLE: PAST AND
PRESENT
This overview of the global N cycle in 1890 (Fig. 3a)
and 1990 (Fig. 3b) is based on data from a number of
sources. The sources of the data on Nr creation have
been discussed previously. Data on atmospheric emis-
sions that are transfers of Nr (as opposed to formation
of Nr) are from van Aardenne et al. (8) with the ex-
ception of marine NH
3
emissions (F. J. Dentener, pers.
comm.). The atmospheric deposition data are based on
Lelieveld and Dentener (22). The estimates of riverine
dissolved inorganic nitrogen (DIN) fluxes are from
Seitzinger and Kroeze (23). Because of different scales
and approaches used to estimate the components of the
N cycle in 1890 and 1990, and due to the absence of
estimates of denitrification and changes in pool size
(e.g. Nr storage), inputs and outputs of Nr are not in
balance. In addition, there is substantial uncertainty in
some of the estimates (e.g. marine NH
3
emissions).
These characteristics of the analysis notwithstanding,
it is clear that the global N cycle underwent a signifi-
67Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
5000
2000
1000
750
500
250
100
50
25
5
fuel combustion which created ~ 21 Tg N yr
–1
, for a total of
~ 140 Tg N yr
–1
. Just as there were large changes in Nr creation
in 1990 relative to 1890, there were also significant changes in
Nr distribution. NH
3
emissions increased from ~ 9 Tg N yr
–1
to
~ 43 Tg N yr
–1
as a consequence of food production; NO
x
emis-
sions increased from ~ 7 Tg N yr
–1
to ~ 36 Tg N yr
–1
from both
energy and food production. The increased emissions resulted
in widespread distribution of Nr to downwind ecosystems as
shown in Figure 4. Transfer of Nr to marine systems also in-
creased. By 1990, riverine DIN fluxes to the coastal ocean had
increased to 20 Tg N yr
–1
and atmospheric N deposition to ma-
rine regions had increased to 27 Tg N yr
–1
. While evidence sug-
gests that most of the riverine N is denitrified in coastal and shelf
environments (24), most of the atmospheric flux is deposited di-
rectly to the open ocean, although a portion of the 27 Tg N yr
–1
is deposited to coastal ocean and shelf regions, with significant
ecological consequences (25).
A key component missing from Figure 3b is the ultimate fate
of the ~ 140 Tg N yr
–1
Nr created by human action in 1990. On
a global basis, Nr created by human action is either accumulated
(stored) or is denitrified. Unfortunately, we are not able to esti-
mate the relative importance of these 2 processes, and until we
are able, we will not be able to determine the rate at which Nr
is accumulating in global systems. We can however, examine
case studies of specific landscape types to obtain a very rough
estimate of Nr accumulation.
We use 2 case studies here. The first is for a landscape type—
global agroecosystems. The second is for specific landscape ar-
eas—16 watersheds that drain the northeastern US coast and that
range from Maine to Virginia. For each case study, Nr introduced
into the system has 3 fates—storage within the system, transfer
to another system, or denitrification to N
2
. Within global
agroecosystems, Smil (9) estimates that ~ 169 Tg N yr
–1
(range
of 151 to 186 Tg N yr
–1
) are added to agroecosystems from nu-
merous sources, including fertilizer, recycling of crop residues,
and animal manures. Of this total, a mean of ~ 14 Tg N yr
–1
1
(range of 11 to 18 Tg N yr
–1
) is denitrified to N
2
, ~ 8% within
agroecosystems. The remainder is recycled back to agroeco-
systems or is transferred to other systems as food and feed, is
discharged to aquatic systems, or is emitted to the atmosphere.
There is significant uncertainty about the amount denitrified, and
it may in fact be a larger number. For example, van Egmond et
al. (26) estimate that for Europe alone, denitrification from
agroecosystems is on the order of 8 Tg N yr
–1
, and Howarth et
al. (27) estimate that it may be as large as ~ 6 Tg N yr
–1
for the
United States.
For watershed landscape units composed of a variable mix-
ture of agroecosystems, forests and urban areas, van Breemen
et al. (28) found that the average N input from atmospheric depo-
sition, fertilizer use, food/feed import and N
2
fixation was 3420
kgN km
–2
yr
–1
, and of that ~ 48% was denitrified (~ 37% in the
landscape; ~ 11% in rivers). Using a different method of analy-
sis in the same watersheds (for rivers only), Seitzinger et al. (29)
estimate that denitrification in rivers may be much larger than
that estimated by van Breeman et al. (28). This difference re-
flects the uncertainty of our knowledge about the rate of con-
version of Nr back to N
2
. It should be noted, that while
denitrification is a large sink in the watershed analysis, much
of the nitrogen still remained in a reactive form, and of the N
that was denitrified, a portion was NO and N
2
O, both environ-
mentally reactive.
In summary, most anthropogenic Nr is not converted to N
2
within agroecosystems. In more complex watershed units, a
larger portion is converted, especially in aquatic ecosystems. In
both examples, the remaining N either accumulates or is dis-
persed via commerce or atmospheric/hydrologic transport to
other environmental systems where it may be stored, denitrified
or further dispersed.
THE NITROGEN CASCADE
About 1965, the rate of human creation of new Nr began to ex-
ceed natural terrestrial creation of Nr. Since conversion of Nr
back to N
2
by denitrification appears not to be keeping pace with
creation of new Nr, it is accumulating in various environmental
reservoirs (e.g. atmosphere, soils, waters). The accumulation of
Nr in environmental reservoirs has significant effects on humans
(30) and ecosystems (25, 26, 31).
There are large uncertainties regarding the rates of Nr accu-
mulation in various reservoirs. This limits our ability to deter-
mine the temporal and spatial distribution of environmental ef-
fects. These uncertainties are even more significant because of
the sequential nature of the effects of Nr on environmental proc-
esses. This sequence of transfers, transformations, and environ-
mental effects is referred to as the nitrogen cascade (32, and Gal-
loway et al., unpublished). As depicted in Figure 5, there are 2
primary sources of Nr—NH
x
creation mainly from food produc-
tion, and NO
x
emissions mainly from energy production. A sin-
gle atom of new NH
x
or NO
x
can alter a wide array of
biogeochemical processes and exchanges among environmental
reservoirs. These processes include:
Figure 4. Global atmospheric
deposition of reactive nitrogen
(Nr) onto the oceans and
continents of the Earth in 1993
(mg N m
–2
yr
–1
). Pers. comm. F.J.
Dentener and based upon
Lelieveld and Dentener (22).
68
© Royal Swedish Academy of Sciences 2002 Ambio Vol. 31 No. 2, March 2002
http://www.ambio.kva.se
– Photochemical transformations and greenhouse effects within
the atmosphere.
– Biological transformations and effects within terrestrial eco-
systems.
– Biological transformations and effects within freshwater and
coastal marine environments.
This sequence of Nr effects is somewhat analogous to the
ability of NO to keep regenerating in the stratosphere and
sequentially destroy one ozone molecule after another.
As new Nr cascades through various environmental reservoirs,
it contributes to a wide variety of changes that impact humans
and ecosystems in different ways in various parts of the world.
Some of these changes are beneficial for society; others are less
so or are detrimental. Table 1 provides a detailed list of these
beneficial and detrimental effects as described in the Summary
Statement for the Second International Nitrogen Conference
(33). In addition to their great variety, another intriguing aspect
of these effects is their linkage through the biogeochemical proc-
esses of the nitrogen cascade. For example, as shown in Figure
5, before being converted back to nonreactive N
2
, a given Nr
atom can in sequence:
i) Increase ozone concentrations in the troposphere.
ii) Decrease atmospheric visibility and increase concentra-
tions of PM2.5 particles.
iii) Increase precipitation acidity.
iv) Increase soil acidity.
v) Increase or decrease forest productivity.
vi) Increase surface water acidity.
vii) Increase hypoxia in coastal waters.
viii) Increase greenhouse warming.
ix) Decrease stratospheric ozone.
A principle feature of the cascade is the accumulation rate of
Nr in environmental systems. This is one of the most important
research questions associated with the impact of humans on the
nitrogen cycle.
REGIONAL ANALYSIS
To assess regional variability of Nr creation and distribution we
divide the world into several regions, Africa, Asia, Europe, Latin
America, North America, and Oceania, as defined by United
Nations Food and Agriculture Organization (FAO) (14). For the
mid-1990s in each region, we have determined the amount of
Nr created by fertilizer production (14), fossil-fuel combustion
(F. J. Dentener, pers. comm.) and rice/legume cultivation (14).
Most fertilizer production occurred in Asia (40.1 Tg N yr
–1
), Eu-
rope (21.6 Tg N yr
-1
) and North America (18.3 Tg N yr
–1
) with
smaller amounts in Latin America, Africa, and Oceania (3.2, 2.5
and 0.4 Tg N yr
–1
, respectively). The other Nr creation process
involved in food production is cultivation-induced BNF. Smil
(9) estimates that ~ 33 Tg N yr
–1
were produced by cultivation
globally in the mid-1990s. The FAO has country and regional
breakdowns of harvested areas for seed legumes, rice and sugar
cane that we use with BNF rates (9) that we use to estimate re-
gional BNF. We calculate these BNF rates from cultivation of
Figure 5. The nitrogen cascade
illustrates the movement of
human-produced reactive
nitrogen (Nr) as it cycles
through various environmental
reservoirs in the atmosphere,
terrestrial ecosystems, and
aquatic ecosystems of the
Earth (Galloway et al. unpubl.).
Table 1. Beneficial and detrimental effects of
reactive nitrogen (Nr).
Direct effects of Nr on human health include:
Increased yields and nutritional quality of the foods needed to meet
dietary requirements and food preferences for growing populations.
Respiratory and cardiac disease induced by exposure to high
concentrations of ozone and fine particulate matter.
Nitrate and nitrite contamination of drinking water leading to the “blue-
baby syndrome” and certain types of cancer.
Blooms of toxic algae, with resultant injury to humans.
Direct effects of Nr on ecosystems include:
Increased productivity of Nr-limited natural ecosystems.
Ozone-induced injury to crop, forest, and natural ecosystems and
predisposition to attack by pathogens and insects.
Acidification and eutrophication effects on forests, soils, and
freshwater aquatic ecosystems.
Eutrophication and hypoxia in coastal ecosystems.
N saturation of soils in forests and other natural ecosystems.
Biodiversity losses in terrestrial and aquatic ecosystems and
invasions by N-loving weeds.
Changes in abundance of beneficial soil organisms that alter
ecosystem functions.
Indirect effects of Nr on other societal values include:
Increased wealth and well being of human populations in many parts
of the world.
Significant changes in patterns of land use.
Regional hazes that decrease visibility at scenic vistas and airports.
Depletion of stratospheric ozone by N
2
O emissions.
Global climate change induced by emissions of N
2
O and formation of
tropospheric ozone.
Damage to useful materials and cultural artifacts by ozone, other
oxidants, and acid deposition.
Long-distance transport of Nr which causes harmful effects in
countries distant from emission sources and/or increased background
concentrations of ozone and fine particulate matter.
In addition to these effects, it is important to recognize that:
The magnitude of Nr flux often determines whether effects are
beneficial or detrimental.
All of these effects are linked by biogeochemical circulation pathways
of Nr.
Nr is easily transformed among reduced and oxidized forms in many
systems. Nr is easily distributed by hydrologic and atmospheric
transport processes.
69Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
FSU. and Latin America (~ 6.0, ~ 3.9 and ~ 5.0 Tg N yr
–1
, re-
spectively). Africa and Oceania created ~< 2 Tg N yr
–1
. Nr crea-
tion by fossil fuel combustion occurred primarily in North
America, Europe and Asia (~ 7.4, ~ 6.6 and ~ 6.4 Tg N yr
–1
,
respectively). Latin America, Africa and Oceania by compari-
son had more modest Nr creation rates, with each being < 1.5
Tg N yr
–1
(Table 2).
There is an additional Nr source for some regions. A portion
of the Nr produced within a region can be exported to other re-
gions. Exports of N-containing fertilizer, plant material (e.g.
grain) and meat from one region will be a source for another
region. To determine the net gain (loss) of N commodities for
the regions we compiled import and export data from the FAO
database (14). Fertilizer was the commodity most often ex-
changed between regions. In 1995, the global production of N
fertilizers was ~ 86 Tg N yr
–1
. Of this amount, ~ 24.9 Tg N yr
–1
were exported to other regions. Over half of the exports were
from Europe (~ 13.2 Tg N yr
–1
). Other regions with significant
exports were Asia (~ 10.7 Tg N yr
–1
) and North America (~ 5.2
Tg N yr
–1
). The primary receiving regions were Asia (~ 7.6 Tg
N yr
–1
) and Europe (~ 6.6 Tg N yr
–1
). Thus, while about ~ 30%
of the fertilizer N produced was exported, the only region that
had a large net loss was Europe (~ 6.6 Tg N yr
–1
). The largest
net gain of any region was for Asia (~ 6.4 Tg N yr
–1
) (Table 2).
The next most frequently exchanged commodity was plant
material, mostly cereal grains. Asia, Europe and Africa had net
gains in N-containing plant material (~ 2.2, ~ 1.0, ~ 0.5 Tg N
yr
–1
, respectively), while North America, Latin America, and
Oceania had net losses (~ 2.8, ~ 0.8, ~ 0.2 Tg N yr
–1
, respec-
tively). Net meat exchange was < 0.1 Tg N yr
–1
for each region.
Summing all three categories (Table 2), Asia gained the most
Nr— ~ 8.7 Tg N yr
–1
. While Oceania and Africa also gained N,
the gains were small (~ 0.3 Tg N yr
–1
and ~ 0.2 Tg N yr
–1
, re-
spectively). Europe and North America had net losses of ~ 5.6
and ~ 3.3 Tg N yr
–1
, respectively. Latin America had a small
net loss. When these net import/exports are added to the Nr crea-
tion in each region (Table 2), North America, with ~ 5% of the
Table 2. Nr creation in mid-1990s for various regions of the world, Tg N yr
–1
.
World Regions Fertilizer Cultivation Combustion Net import/ Total
production export
Africa 2.5 1.8 0.8 0.2 5.3
Asia 40.1 13.7 6.4 8.7 68.9
Europe + FSU 21.6 3.9 6.6 –5.6 26.5
Latin America 3.2 5.0 1.4 –0.2 9.4
North America 18.3 6.0 7.4 –3.3 28.4
Oceania 0.4 1.1 0.4 0.3 2.2
World ~ 86 ~ 30 ~ 23 0.1 ~ 140
Table 3. Regional per capita Nr creation in mid-1990s
during food and energy production, kg N person
–1
yr
–1
.
Regions Food Energy Total
Africa 5.7 1.1 6.8
Asia 15 1.8 17
Europe & FSU 35 9.1 44
Latin America 16 2.8 19
North America 80 24 100
Oceania 50 13 63
World 20 3.9 24
world’s population, is responsible for creation of ~ 20% of the
world’s Nr. Africa, with ~ 13% of the world’s population, is re-
sponsible for ~ 6% of the world’s Nr.
Given these regional differences, it is also interesting to ex-
press Nr creation and use on a per capita basis (calculated from
Table 2 (not including net import/export) and FAO population
data (14)), to illustrate the average amount of Nr mobilized per
person, by region (Table 3). At one extreme North America mo-
bilizes ~ 100 kg N person
–1
yr
–1
; at the other extreme, Africa,
mobilizes about an order of magnitude less, ~ 7 kgN person
–1
yr
–1
(Fig. 6). In all regions, food production is larger than en-
ergy production, and the primary cause for the regional differ-
ences are the amounts of N mobilized per capita in the produc-
tion of food. In North America, it is ~ 80 kgN person
–1
yr
–1
; in
Africa it is ~ 6 kgN person
–1
yr
–1
. Remembering back to the sec-
tion on ‘Body vs. Being’, these values show which regions are
responsible for Nr creation in excess of what is needed for hu-
man body sustenance.
This regional analysis focuses on Nr creation and interregional
exchange through commerce. Very detailed regional case stud-
ies are presented for Europe (26), United States (27) and Asia
(34) in this issue of Ambio.
FUTURE
Nr creation by human action will continue to increase in the fu-
ture as global populations grow. Even after they peak, perhaps
sometime in this century (35), Nr creation will still most likely
continue to increase due to growth in per capita resource use.
How high will the Nr-creation rate go? In 1990, it was ~ 140
Tg N yr
–1
, and the average per capita Nr-creation rate was ~ 24
kg N person
–1
yr
–1
, and ranged from ~ 7 kg N person
–1
yr
–1
in
Africa to ~ 100 kg N person
–1
yr
–1
in North America (Fig. 6).
If the global population peaks at ~ 8.9 billion people (estimate
of global population in 2050; United Nations (36)) and if all peo-
ple had the same per capita Nr-creation rate from food and en-
ergy production as North America in 1990 (~ 100 kg N person
–
1
yr
–1
), then the total Nr-creation rate would be ~ 900 Tg N yr
–1
,
Figure 6. Comparison of reactive nitrogen (Nr) creation rates for various regions of the world.
The left bar shows the total amount of Nr created in each region in 1995 (Tg N yr
–1
). The right bar
shows the amount of Nr created in each region in 1995 on a per capita basis (kg N person
–1
yr
–1
).
seed legumes, rice, and sugar cane: Africa,
1.8; Asia, 9.2; Europe + Former Soviet Un-
ion (FSU), 0.4; Latin America, 3.0; North
America, 2.5; Oceania 0.3 Tg N yr
–1
). How-
ever, FAO does not have equivalent data for
N fixation by leguminous cover crops and
non-Rhizobium diazotrophs that can be used
to divide by region the ~ 14 Tg N yr
–1
pro-
duced annually from these 2 sources (9). But,
based on an analysis of fixation for selected
major countries, Smil (V. Smil, pers. comm.)
suggests that the apportionment of the 14 Tg
N yr
–1
among the regions is ~ 4.5, 3.5, 2.0,
3.5, and 0.8 for Asia, Europe + FSU, Latin
America, North America, and Oceania, re-
spectively, with an uncertainty of about 25%
around these estimates. Summing, we found
that cultivation-induced BNF was focused in
Asia (~ 13.7 Tg N yr
–1
), with more modest
creation rates in North America, Europe +
70
© Royal Swedish Academy of Sciences 2002 Ambio Vol. 31 No. 2, March 2002
http://www.ambio.kva.se
watercourses with little or no concern about the associated (and
much larger) air emissions of volatile ammonia and amines. All
oxidized, reduced, and organic forms of Nr participate in a va-
riety of chemical and physical transformations in the atmosphere.
As indicated in Table 1, they also can have a long series of ben-
eficial and detrimental biological effects once they are transferred
into terrestrial and aquatic ecosystems as indicated in the nitro-
gen cascade (Fig. 5).
The time has come to develop and implement a Total Reac-
tive Nitrogen Approach (Total Nr Approach), rather than con-
tinue to consider nitrogen-oxide pollution and ammonia pollu-
tion in isolation from each other and from other aspects of air-
and water-quality management. A Total Nr Approach is firmly
grounded in the following biological principles (48–50):
i) Although there are transitory differences in rates of uptake
and assimilation, all oxidized, reduced, and organic forms
of Nr have substantially similar influences on the general pro-
ductivity of the terrestrial, aquatic, and livestock-dominated
ecosystems systems in which they are deposited and assimi-
lated. This is true because at least one or another (and some-
times many) of the various plants, animals, microbes, and
insects in terrestrial and aquatic ecosystems take up all oxi-
dized, reduced, and organic forms of Nr. After initial uptake
and assimilation, these various forms of Nr are readily trans-
formed and exchanged with other organisms and compart-
ments within a given landscape or watershed.
ii) When transferred into ecosystems in less than optimal
amounts, oxidized, reduced, organic forms of Nr are biologi-
cally available and increase the productivity of the system.
iii) When applied in more than optimal amounts, however, all
biologically active forms of Nr contribute to the wide vari-
ety of detrimental effects listed in Table 1.
iv) The total supply of Nr in terrestrial and aquatic ecosystems
is a complex function of the atmospheric, terrestrial, and
aquatic transfer, and transformation processes outlined in the
nitrogen cascade (Fig. 5).
A Total Nr Approach is especially important in the context
of recent international negotiations: i) The recommendations of
Grennfelt et al. (51) for multiple-pollutant perspectives in the
new nitrogen protocol; and ii) acceptance of the “multiple-pol-
lutant/multiple-effects” (Gothenburg Protocol) by the now 31
North American and European nations that signed this protocol
following its final negotiation in December 1999 (52).
CONCLUSIONS
Over the course of about 2 centuries, human involvement with
N progressed from its discovery in the late-18
th
century to hu-
Figure 7. Comparison of contemporary and possible future reactive nitrogen (Nr) creation
rates in various regions of the world. The left bar shows the total amount of Nr created in each
region in 1995 (Tg N yr
–1
). The right bar shows the amount of Nr that would be created in each
region at the time of maximum projected human population of the Earth (~ 8.9 billion people)
assuming that the average Nr creation rate in North America in 1995 (~ 100 kg N person
–1
yr
–1
)
was achieved in all regions of the world.
West (40), Oenema and Pietrzak (41), Roy et al. (42) and Smil
(21). Policy options are presented in some of these papers as well
as in Melillo and Cowling (43).
As is noted in other papers, for management to be effective,
it must take into account all aspects of Nr. The next section
presents the case for developing a Total Nr Approach for man-
agement of Nr.
DEVELOPMENT OF A CONCEPT OF OPTIMUM Nr
MANAGEMENT FOR SOCIETY
In his most famous book, “Future Shock,” Toffler (44) identi-
fied 3 different types of futures, that he believed innovative
democratic societies should consider very carefully:
i) Probable futures: Hopes and aspirations of society that are
largely an extension of a “business as usual” sense of what
the future might hold.
ii) Possible futures: Exploration of all possible outcomes that
a given society might wish to explore as possibilities for its
future.
iii) Preferable futures: Optimum outcomes that probably can be
achieved only as a result of focused and well-disciplined ef-
forts to fulfill mutually agreed upon goals and dreams which
are consonant with the natural and human resources avail-
able to society.
An excellent example of efforts to evaluate ‘preferable futures’
is provided by the computer simulation game, NitroGenius (45),
developed for the Dutch government, and presented at the Sec-
ond International Nitrogen Conference.
In evaluating alternative choices about management of air and
water quality in the context of other important societal goals,
enlightened societies will want to consider Toffler’s suggestions
and thus go beyond “business as usual” perspectives, look ear-
nestly at a wide range of “possibilities,” and work hard to de-
fine and implement “preferable” options that are both prudent
and realistic for the long-term as well as for the short-term fu-
tures of society (46, 47).
So far, most of the voluntary recommended management prac-
tices and the mandated rules and regulations for management of
Nr have been developed and administered separately. For ex-
ample, air emissions of NO
x
were first regulated because NO
x
is an important precursor of ozone and later because it also con-
tributes to acidification of soils and surface waters. Similarly,
air emissions of ammonia first became a pollutant of concern
because ammonia contributes to acidification processes. Also,
most guidance for prevention of nitrogen emissions from con-
fined animal feeding operations in North America have been de-
veloped and administered with emphasis on direct discharges to
with about half occurring in Asia (Fig. 7).
Given the concerns about Nr, it is very un-
likely that this value will be reached. What
the final maximum Nr-creation rate turns
out to be, however, will depend to a very
large extent on how the world manages its
use of nitrogen for food production and its
control of N in energy production.
Thus, there is ample opportunity for crea-
tive management of Nr in the development
of strategies that will allow for optimization
of food and energy production while also
optimizing environmental health. Several
papers in this volume address the issue of
Nr management to maximize food and en-
ergy production, and protect the health of
people and ecosystems. Management of en-
ergy producing systems is discussed by
Moomaw (37) and Bradley and Jones (38).
For food production, management issues are
discussed in Cassman et al. (39), Fixen and
71Ambio Vol. 31 No. 2, March 2002 © Royal Swedish Academy of Sciences 2002
http://www.ambio.kva.se
man dominance of its terrestrial cycle in the late-20
th
century.
The production of food and energy, so critical to human survival,
has resulted in substantial increases in the amount of Nr in en-
vironmental reservoirs. These increases have a number of effects,
both positive and negative, which due to the biogeochemical
characteristics of Nr, can occur in sequence as Nr cascades
through the environment.
While the benefits of increasing amounts of Nr are numerous,
all of the Nr that is created by human action is eventually re-
leased into the environment. A critical topic for research is de-
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54. We are grateful for the comments of three anonymous reviewers, and the assistance of
Vaclav Smil. We are also appreciative of the suggestions from authors of other papers
in this volume. Cari Furiness provided her usual thorough editorial assistance, and Mary
Ann Seifert and Sue Donovan were instrumental in putting the paper into the correct
format. JNG is grateful to The Ecosystems Center of the Marine Biological Labora-
tory, and the Woods Hole Oceanographic Institution for providing a sabbatical home
to write this paper, and to the University of Virginia for the Sesquicentennial Fellow-
ship. We are both very grateful for the opportunity to serve as Chairpersons for the
Second International Nitrogen Conference. It has been one of the most stimulating ex-
periences of our careers.
termination of the fate of this Nr. Where is it going? How much
is stored? How much is denitrified? We will not be able to de-
termine the impact of Nr mobilization on human and environ-
mental systems until we can account for its fate. Another criti-
cal topic for research is how can we manage Nr more effectively?
Specifically, how can we eliminate the creation of Nr by energy
production? How can we decrease the amount of nitrogen re-
leased during food production?
These critical issues will require a new way of examining how
people manage the environment and their use of resources.
James N. Galloway is professor of environmental sciences
at the University of Virginia, USA. His research on
biogeochemistry includes the natural and anthropogenic
controls on chemical cycles at the watershed, regional and
global scales. His current research focuses on beneficial
and detrimental effects of reactive nitrogen as it cascades
among environmental reservoirs in the atmosphere and
biosphere of the Earth. His address: Department of
Environmental Sciences, University of Virginia,
Charlottesville, VA 22903, USA.
E-mail: jng@virginia.edu
Ellis Cowling is University Distinguished Professor At-Large
at North Carolina State University. His interests in nitrogen
began with his doctoral dissertation research on
Nitrogen in
Forest Trees and Its Role in Wood Deterioration
at the
University of Uppsala, Sweden and has continued in his
leadership roles in the US National Acid Precipitation
Assessment Program and the Southern Oxidants Study.
His address: North Carolina State University, Raleigh,
NC 27605, USA.
E-mail: ellis
–
cowling@ncsu.edu
