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OCR for page 6001
Proc. Natl. Acad. Sci. USA
Vol. 96, pp. 6001-6008, May 1999
Colloquium Paper
This paper was presented at the National Academy of Sciences colloquium "Plants and Population: Is There Time?"
held December 5-6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.
Nitrogen management and the future of food: Lessons from the
management of energy and carbon
ROBERT H. SOCOLOW*
Center for Energy and Environmental Studies, Princeton University, Princeton, NJ 08544
ABSTRACT The food system dominates anthropogenic
disruption of the nitrogen cycle by generating excess fixed
nitrogen. Excess fixed nitrogen, in various guises, augments
the greenhouse effect, diminishes stratospheric ozone, pro-
motes smog, contaminates drinking water, acidifies rain,
eutrophies bays and estuaries, and stresses ecosystems. Yet, to
date, regulatory efforts to limit these disruptions largely
ignore the food system. There are many parallels between food
and energy. Food is to nitrogen as energy is to carbon.
Nitrogen fertilizer is analogous to fossil fuel. Organic agri-
culture and agricultural biotechnology play roles analogous to
renewable energy and nuclear power in political discourse.
Nutrition research resembles energy end-use analysis. Meat is
the electricity of food. As the agriculture and food system
evolves to contain its impacts on the nitrogen cycle, several
lessons can be extracted from energy and carbon: (i) set the
goal of ecosystem stabilization; (ii) search the entire produc-
tion and consumption system (grain, livestock food distribu-
tion, and diet) for opportunities to improve efficiency; (iii)
implement cap-and-trade systems for fixed nitrogen; (iv)
expand research at the intersection of agriculture and ecology,
and (v) focus on the food choices of the prosperous. There are
important nitrogen-carbon links. The global increase in fixed
nitrogen may be fertilizing the Earth, transferring significant
amounts of carbon from the atmosphere to the biosphere, and
mitigating global warming. A modern biofuels industry some-
day may produce biofuels from crop residues or dedicated
energy crops, reducing the rate of fossil fuel use, while losses
of nitrogen and other nutrients are minimized.
The agriculture and food system disrupts the biogeochemical
nitrogen cycle at various spatial scales. Limiting the impact of
the agriculture and food system on the nitrogen cycle is
increasingly important, as that system grows to feed a larger
and more affluent world population.
Managing the food-nitrogen connection is likely to resemble
managing the energy-carbon connection, a task that already
has begun. The parallels between food and energy are myriad.
In both the food and energy systems, alarms regarding a crisis
of global supply were sounded in the 1970s, innovations and
adaptations followed that permitted growth to continue, and
the focus now is on addressing adverse impacts of further
expansions of supply. Problems of scarcity share the stage with
problems of abundance.
This paper reviews the nitrogen cycle, its disruptions by
human activity, and some of the adverse environmental con-
sequences of these disruptions. It then suggests principles,
extracted from the energy-and-carbon arena, that might guide
modification of the agriculture and food system to increase its
responsiveness to nitrogen management objectives.
PNAS is available online at www.pnas.org.
How the Nitrogen Cycle Works and How It Is Being
Disrupted
The Nitrogen Cycle. Given that extensive introductions to
the biogeochemical nitrogen cycle are found elsewhere (1-5),
a quick tour here may suffice. Nitrogen is found in three forms.
It is bound to itself in a two-atom molecule, dinitrogen, or N2;
this form is the most abundant, but it is almost unavailable to
life because it is so stable that only a few specialized bacteria
(and lightning) can break it apart. Nitrogen is bound to carbon,
as organic nitrogen, in a magnificent variety of organic mol-
ecules, critical to life and present long after death, including
proteins and their component amino acids. And it is bound
neither to itself nor to carbon, in nitrogen nutrients. Nitrogen
nutrients are relatively small molecules, both nitrogen ions and
nitrogen gases. The principal nitrogen ions are ammonium
(NH4+) and nitrate (NORM. The nitrogen gases include am-
monia (NH3); various oxides of nitrogen, including nitric oxide
(NO), nitrogen dioxide (NO2), dinitrogen pentoxide (N2O5),
and nitrous oxide (N2O); and nitric acid vapor (HNO3).
A specialized vocabulary describes the transformations from
one form to another. Fixation is the process of making N2 into
nitrogen nutrients (largely NH4+), and denitrification (in
effect, unfixing) is the process of rebuilding N2 from nitrogen
nutrients (largely NO3-). Nitrification oxidizes ammonium to
nitrate. (A complication: Side reactions of both Vitrification
and denitrification produce N2O.) Assimilation and immobi-
lization are the processes by which nutrients become organic
nitrogen (plants assimilate, microorganisms immobilize), and
mineralization is the process by which organic nitrogen is
decomposed back into nitrogen nutrients. Assimilation, im-
mobilization, and mineralization are capabilities found widely
in nature, but fixation and denitrification can be accomplished
only by specialized microorganisms.
Both air routes and water routes connect nutrient systems
across large distances. Denitrification, mineralization, and
vitrification all produce nitrogen gases. Once volatilized into
the atmosphere, these gases undergo further chemical trans-
formations before returning to the Earth's surface by wet or
dry deposition. Alternatively, nitrogen nutrients and organic
nitrogen can be leached into groundwater or carried in runoff
into surface water, then transported down waterways in solu-
tion or attached to solid particles.
The nitrogen cycle is captured quantitatively by the magni-
tudes of the stocks of nitrogen in the various biological and
geophysical "reservoirs" "measured in millions of metric tons
of nitrogen, Mt(N), for example] and the flows of nitrogen
between pairs of reservoirs (in Mt(N)/yr). The stock of N2 in
the atmosphere is so large, 3.9 x 10~5 Mt(N), as to be
Abbreviations: Mt(N), metric tons of nitrogen; Mt(C), metric tons of
carbon; ha, hectare.
*To whom reprint requests should be addressed. e-mail: socolow@
princeton.edu.
6001
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6002 Colloquium Paper: Socolow
effectively infinite. The stock of terrestrial organic nitrogen is
about 100,000 Mt(N); very little terrestrial fixed nitrogen is in
the form of nutrient, because uptake by plants is rapid. Only
4% of the 100,000 Mt(N) of terrestrial organic nitrogen is in
living organisms, and the rest is in dead organic matter (5~. Of
the terrestrial dead organic matter, roughly 15% is labile, and
85% is recalcitrant, the distinction referring to the ease of
mineralization. The stock of fixed nitrogen in the ocean, about
half nutrients and about half dead organic matter, is roughly
10 times larger than the stock of terrestrial fixed nitrogen (5, 6~.
Evidence for Human Impact on a Global Scale. The con-
centration of nitrous oxide in the atmosphere gives indirect
information about human impacts on the nitrogen cycle.
Records from ice cores reveal-that the concentration of nitrous
oxide fluctuated only a few percent in the period from 2,000
years ago until about a century ago, when a statistically
significant upward climb began. The current concentration,-
about 310 parts per-billion by volume (ppbv), is about 10%
higher than the average value before this century, and the
current rate of increase is about 0.8 ppbv per year, or 0.3% per
year, corresponding to a flow of 4 Mt(N)/yr (5~. The stable
concentration in earlier times and the rising concentration in
the past century are presumed to be evidence that a stable
dynamic equilibrium governed the flows of nitrogen among
soils, waterways, oceans, and the atmosphere until human
activity was boisterous enough to create a detectable signal. A
similar story is told by the ice-core record of the atmospheric
concentration of carbon dioxide (CON: the concentration
started its upward climb 200 years ago, is currently climbing
0.5% per year, and is now about 30% above its earlier average
value. The earlier period of dynamic equilibrium and nearly
constant atmospheric concentration is called the preindustrial
period; its features are crude averages over several centuries of
data, ending roughly in 1800.
Specifically, for the preindustrial global nitrogen cycle to
have been in dynamic equilibrium requires a constant flow of
fixed nitrogen (i) through the fixed-nitrogen subcycle, where
nutrient is transformed into organic nitrogen and back
(through a loop of assimilation, death, and mineralization);
and (~ii) through the fixing-unfixing subcycle, where N2 is
transformed into nutrient and back. Quantitatively, and re-
stricting attention to the terrestrial component of these sub-
cycles, 1,200 Mt(N)/yr flowed through the fixed nitrogen cycle
and 140 Mt(N)/yr f lowed through the fixing-unfixing subcycle.
Ocean and land nitrogen cycles are linked by river runoff, and
coastal zones are active regions of nitrogen transformation.
Ocean and land nitrogen cycles also are linked by atmospheric
transport of nitrogen gases between land and sea. The flows
that form the ocean components of the global nitrogen cycle
are poorly known (5~.
The rate at which nitrogen is being fixed on land today is
approximately 300 Mt(N)/yr, roughly double its preindustrial
value. Thus, the incremental fixation today from the global
industrial and agricultural system of human beings is roughly
equal to natural fixation in preindustrial times. This startling
result captures the essence of the human impact on the
nitrogen cycle. Its consequences depend strongly on the extent
to which denitrification has kept pace with fixation. Unfortu-
nately, a quantitative understanding of denitrification rates in
various managed and unmanaged terrestrial and aquatic
environments is largely missing, probably the biggest obsta-
cle thwarting accurate modeling of the present-day nitrogen
cycle (3~.
Anthropogenic Additions of Fixed Nitrogen. The additional
flow of approximately 160 Mt(N)/yr from human nitrogen-
fixation activity has three principal components. The two
largest are directly related to agriculture: the synthesis of
ammonia, largely for nitrogen fertilizer, and land use that
enhances biological fixation. Ammonia synthesis is accurately
known to be contributing about 95 Mt(N)/yr globally, of which
Proc. Natl. Acad. Sci. USA 96 (1999J
80 Mt(N)/yr is incorporated into synthetic nitrogen fertilizer,
and the rest is "consumed by chemical industries and lost
during processing and transportation" (7~. The third contrib-
utor is high-temperature combustion, estimated, also very
roughly, at 30 Mt(N)/yr (8, 9~. I examine each of these three
in turn.
Fertilizer. Nitrogen fertilizer is made from ammonia, and
ammonia is made, in effect, fixed, from nitrogen in the air. An
ammonia factory requires very high pressures and moderately
high temperatures to accomplish what bacteria accomplish at
ordinary pressures and temperatures. The single human ac-
tivity of nitrogen fertilizer production provides more than half
of all anthropogenic fixed nitrogen. Fertilizer is the fossil fuel
of food.
Fig. 1A displays 35 years of global nitrogen fertilizer use
(1961-1995), disaggregated into 10 geographical regions (In-
ternational Fertilizer Industry Association, http.//www.fertil-
izer.org.~. The rate of global nitrogen fertilizer use crossed 20
Mt(N) in 1965, 40 Mt(N) in 1973, and 60 Mt(N) in 1979. It
remained within a band from 75 Mt(N) to 85 Mt(N) from 1986
to 1995, the consequence of continuous growth of consump-
tion in Asia and a precipitous fall in consumption in the former
Soviet Union and Eastern Europe.
The plausibility of both saturation effects and upward
pressures complicates attempts to predict future consump-
tion of nitrogen fertilizer (10~. The saturation in nitrogen
fertilizer use in North America and Western Europe seen in
Fig. 1A reflects fundamental physiological limits to yields
and diminishing returns to single-factor inputs. A falling
ratio of nitrogen fertilizer use to gross domestic product
should be anticipated, inasmuch as nitrogen fertilizer con-
tributes only to the production of a commodity and not to the
downstream processing and services that account for an
increasing fraction of wealth as incomes rise. By contrast,
energy is a needed input at every stage in a complex
economy, and hence has fewer built-in features leading to
saturation. Saturation in fertilizer use will be reinforced as
fertilizer subsidies are removed and external environmental
costs are internalized in the fertilizer price.
Other pressures act to counter saturation. Upward pressure
on nitrogen fertilizer use will be felt, as latent demand in many
developing countries is expressed. Fig. L4 shows that the
growth in fertilizer use across the developing world has been
very uneven, and comparisons of fertilizer use on the same
crop across countries confirms that fertilizer use and yield are
correlated (ref. 11; http://www.fertilizer.org/CROPS/
CROPS/harris.htm.~. Upward pressure also will be felt if
agricultural biotechnology continues to raise ceilings on yield
potential with new crop variants dependent on nitrogen. Still
other pressure may come from an expansion of fertilizer use
on commercial forests and nonfood crops. As an alternative to
fossil fuel, fast-growing energy crops may be established on
dedicated, fertilized plantations.
Nitrogen's share, by weight, of total fertilizer (nitrogen plus
phosphorus plus potassium) has climbed steadily; today, ni-
trogen's share is about 60%, in sharp contrast to 1960, when
roughly equal amounts of nitrogen, phosphorus, and potas-
sium were applied. This phenomenon reflects a comparative
advantage of nitrogen fertilizer resulting from both plant
physiology and economics. It also reflects the unavailability of
phosphorus or potassium in some parts of the world, leading
to inappropriate ratios of application (ref. 12 and http://
www.fertilizer.org/PUBLISH/PUBENV.~.
It is interesting to compare the history of the use of nitrogen
fertilizer and fossil fuels. Fig. 1B mimics Fig. 1A: the carbon
content of fossil fuel use is shown for the same 10 geographical
subregions and the same time period (ref. 50; Carbon Dioxide
Information and Analysis Center, http://cdiac.esd.ornl.gov/
ndps/ndpO30.html). Total global fossil-carbon use grew more
slowly than total fertilizer use, crossing 3,000 million metric
OCR for page 6003
CO11OqUiUm Paper: SOCO1OW
so I: ..i ,
80
1
60 ~
1
so ~
an
an
in
NItrO90 In Fertilizer 1961-95
`,, (A)
o
70 1 ~
~ '
~0
C
O
._
._
5
Proc. Natl. Acad. Sci. USA 96 (1999J 6003
7,000 i
6.000,
Ci
~ O
Carbon in Fossil Fuel 196195
tB)
__
__
__
1961 t~ 1~1 1976 1~1
D North America @l Western Europe
oil Corner Soviet tJnion ~ Near East
|3 South and Southeast Asia ~ Socialist Ash
Togo 1 ~
t ~
, ~
1 ~
4,000 1 -
Oceania and Japan [1 Eastern Europe
Afrca ~ Latin Arner~a
FIG. 1. Comparable global data on release of nitrogen in fertilizer and release of carbon in fossil fuel, 1961-1995, with site of release
disaggregated into 10 world regions. (A) Nitrogen in fertilizer; data from http://www.fertilizer.org. (B) Carbon in fossil fuel; data from
http://cdiac.esd.ornl.gov/ndps/ndpO30.html.
tons of carbon [Mt(C)] in 1965 and 4,000 Mt(C) in 1971, then
remaining within a band between 4,800 and 5,100 Mt(C) from
1977 to 1984 and within a second band between 5,800 and
6,000 Mt(C) between 1988 and 1994. Growth of fossil-carbon
use was slowed substantially by investments in energy effi-
ciency.
Comparing Fig. 1 A and B reveals that developing-country
Asia gained global share more rapidly for nitrogen fertilizer
than for fossil carbon. From 1961 to 1995, its nitrogen share
climbed from 14~o to 50% whereas its carbon share climbed
only from 9% to 26%. In 1995, the nitrogen shares for North
America and Western Europe were 15% and 12%, respec-
tively, whereas the corresponding carbon shares were larger,
25% and 14%. In the former Soviet Union and in Eastern
Europe nitrogen fertilizer fell far more than fossil-carbon use
during the last years shown: In the former Soviet Union the
1995 level of nitrogen fertilizer use was 19% of the 1987 level,
and in Eastern Europe it was 47% of the 1987 level, whereas
the 1995 levels of fossil-carbon use were 70% and 63% of 1987
levels, respectively. Careful study of the fall in fertilizer use in
the former Soviet Union and in Eastern Europe seems war-
ranted.
Land use. Land devoted to legumes, such as soybean and
alfalfa, is the site of anthropogenic fixed-nitrogen production.
Legumes are extraordinary, relative to other crops, in hosting
nitrogen-fixing microorganisms in their roots; legumes are
botanical fertilizers. At harvest, there is far more nitrogen in
legumes than in other crops: soybeans are about No nitrogen
(dry mass), wheat is 2%, rice is 1%. Land devoted to wet rice
cultivation promotes asymbiotic nitrogen fixation, and thus is
another site of anthropogenic fixed-nitrogen production.
Schlesinger (5), citing Burns and Hardy (13) and including only
legumes, estimates total anthropogenic land-use-related nitro-
gen fixation to be 40 Mt(N). Galloway (8), including both
legumes and rice, makes the same estimate. Successive im-
provements in such estimates can be imagined, which compare
preindustrial and contemporary nitrogen fixation rates for
more and more kinds of land-use change. Included, for exam-
ple, would be land converted from forests to fields.
Land use also affects denitrification. Agricultural practices
that reduce anaerobic environments, such as plowing (which
aerates the soil) and draining wetlands, decrease denitrifica-
tion, whereas irrigation increases denitrification. Denitrifica-
tion also generally increases where fertilizer is applied, where
legumes are planted, and where crops accelerate the miner-
alization of recalcitrant nitrogen in the soil. Greater burning of
biological material also increases denitrification, because some
of the nitrogen in biological material (wood, for example)
recombines into N2 in flames, a process known as pyrodeni-
trification (2~.
The management of nitrogen, like the management of
carbon, is likely to evolve from a focus only on sources to a
balanced focus on sources and sinks. A strategy of engineered
denitrification to reduce fixed-nitrogen build-up might ensue,
based on manipulating land use to enhance natural denitri-
fication processes. Presuming the simultaneous goal of
managing the global greenhouse, such a strategy would entail
only options with favorable ratios of wanted N2 to un-
wanted N2O.
Combustion. Where the temperature of combustion exceeds
about 1,500°C, there is enough concentrated energy to break
apart atmospheric N2 and to form nitrogen oxides (14~.
Nitrogen oxide production also results as the "fuel nitrogen"
in fossil fuels is burned. Estimating the rate of nitrogen fixation
caused by anthropogenic combustion requires taking into
account both the amount of combustion and the amount of
pollution control. Control of nitrogen oxide emissions is
increasingly widespread and increasingly strict.
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6004 Colloquium Paper: Socolow
Why the Increase in Stocks of Fixed Nitrogen Is
Troublesome
Schematically, one can identify seven distinct adverse impacts
of anthropogenic disruption of the nitrogen cycle, two ex-
pressed at the global scale and five at the regional scale. The
two global impacts are caused by nitrous oxide in the atmo-
sphere both contributing to the greenhouse effect and reduc-
ing the concentration of stratospheric ozone. Two of the five
regional effects have direct impacts on public health: air
pollution and unhealthy nitrate concentrations in drinking
water. The other three regional effects are mediated by
ecological processes: acid deposition, eutrophication of bays
and estuaries, and ecosystem disruption resulting from uneven
responses to nitrogen fertilization across species.
These nitrogen effects can "cascade" (8~. A nitrogen atom
leaking away from an agricultural area can contribute to an
air pollution problem over a city, then to a nitrate concen-
tration problem in a municipal water supply, then to an
acidification problem in a lake, then to a eutrophication
problem in an estuary, and then to the destruction of ozone
in the stratosphere. Such sequences, of course, can be
interspersed with second passes through the agriculture and
food system: through a cycle of fodder, cow, and manure, for
example.
I review each of the seven impacts briefly below. Note that
in six of the seven instances (all except ecosystem disruption)
a regulatory regime either is already in place or is being
designed.
Nitrous Oxide (N2O) Is a Greenhouse Gas. Because N2O
has a long (120-year) residence time in the atmosphere and
absorbs IR radiation, it is the one nitrogen gas emitted into the
atmosphere that contributes significantly to the greenhouse
effect: It is the fourth largest contributor to the natural
greenhouse effect, after water vapor, carbon dioxide, and
methane. The increase in N2O concentration since preindus-
trial times contributes about one-fifteenth as much to the
greenhouse effect as the increase in CO2 concentration in the
same period; about one N2O molecule has been added for
every 3,000 CO2 molecules, but each is about 200 times as
effective. Nitrous oxide is included explicitly in international
climate agreements.
Nitrous Oxide Depletes Stratospheric Ozone. The long
atmospheric residence time of nitrous oxide is a consequence
of its lack of reactivity in the troposphere and its very low
solubility in water. Nitrous oxide is destroyed only in the
stratosphere, where energetic UV light breaks it apart. One
product of its decomposition is nitric oxide (NO), which acts
catalytically to lower the concentration of stratospheric ozone
(15~. The engines of subsonic and supersonic aircraft traveling
at high altitudes also emit nitric oxide in regions affecting
stratospheric ozone. Current international assessments of the
impact of aircraft nitric-oxide emissions on stratospheric
ozone are expected to influence the near-term future of
supersonic aircraft, as well as the regulatory regime for engine
emissions of subsonic aircraft. Thus, because agriculture and
aviation share common stratospheric chemistry, agriculture is
enmeshed for the indefinite future in a high-stakes aerospace
debate.
Nitrogen Gases Generate Air Pollution. Because of their
high reactivity in the atmosphere, nitric oxide (NO) and
nitrogen dioxide (NO2), collectively called NOX, control the
production of tropospheric ozone. Nitrogen gases (both am-
monia and nitrogen oxides) are also precursors of very small
particulates that travel long distances in the atmosphere and
that find their way deep into the lung when inhaled (51~. The
regulation of NOX and tropospheric ozone is at the core of air
pollution control in the United States. Emerging attention to
very small particulates may lead to further regulations on
nitrogen emissions.
Proc. Natl. Acad. Sci. USA 96 (1999J
The Concentration of Nitrate Ions in Drinking Water Can
Be a Threat to Infant Health. Nitrite ions (NO2-) in blood
can inactivate hemoglobin, with dangerous consequences.
The inactivation occurs because nitrite ions change hemo-
globin, whose iron is doubly charged (Fe++) and can carry
oxygen, into me/hemoglobin, whose iron is triply charged
(Fe+++) and cannot carry oxygen. Infants younger than
about 3 months are particularly at risk, for reasons that are
not fully understood. The American Academy of Pediatrics
speculates that fetal hemoglobin (which remains in the infant
for the first few months of life) "may be more susceptible to
oxidation to methemoglobin by nitrite" (ref. 16; see http://
www.aap.org/policy/356.html). Because the nitrite ions are
formed in the gastrointestinal tract by the chemical reduction
of nitrate ions (NO3-), the target of regulation is nitrate
intake (17~. The U.S. Environmental Protection Agency
estimated in 1992 that 66,000 at-risk infants were drinking
water whose nitrate concentration exceeded the U.S. health
standard, 10 mg of nitrogen as nitrate (NO3--N) per liter of
water (18~. Several water treatment options are available, all
quite costly (18~.
Nitrogen Oxides Emitted into the Atmosphere Contribute
to Acid Deposition. Acid deposition encompasses two related
phenomena by which acidity is transferred from the atmo-
sphere to the Earth's surface: acid precipitation (including
fog, rain, and snow) and dry deposition. The two principal
contributors to acid deposition are nitrate and sulfate ions.
Because precipitation is acidic even in the absence of air
pollution (as a result of the effects of carbon dioxide and
other gases on moisture in the atmosphere), acid precipita-
tion is a term reserved for precipitation that is made still
more acidic by pollution. Damage from acid deposition has
been widely explored, and adverse consequences for lakes,
forests, and buildings have been documented. To date,
regulatory intervention to reduce acid deposition has fo-
cused far more on sulfate than nitrate, largely because a
greater fraction of atmospheric sulfate arises from large
emitters.
High Nitrate Concentrations in Aquatic Ecosystems Can
Lead to Eutrophication. Nitrogen is the limiting nutrient in
many aquatic ecosystems, especially estuaries and bays, and
thus the addition of nitrogen can lead to eutrophication, or
excessive plant growth, followed by the depletion of dissolved
oxygen and the development of aquatic "dead zones" where
these plants decay (19~. Because phosphorus, rather than
nitrogen, is usually the limiting nutrient in fresh-water eco-
systems, nitrate added to watersheds in their headwaters can
be carried almost all the way to the sea before causing its first
visible damage, thereby separating cause and effect both in
space and time.
An example is the hypoxic zone in the Gulf of Mexico off
Louisiana, presumed to be brought about by agriculture in
the Mississippi River watershed. A region defined by a
dissolved oxygen concentration of less than 2 mg/liter,
unable to sustain most forms of life, this hypoxic zone grows
along the bottom of the gulf each summer as the gulf
stratifies, plankton in abundance die and sink, and the
dissolved oxygen at lower depths is consumed. The area of
the hypoxic zone has been approximately 13,000 square km
in recent years. In drought years the area is smaller and in
flood years the area is larger, compelling evidence that
something is carried into the gulf that promotes the growth
and subsequent decay of plankton. Excess nitrogen from
fertilized fields and livestock in the Great Plains is impli-
cated. An interagency Mississippi River/Gulf of Mexico
Watershed Nutrient Task Force has been established to
assist policy-making (ref. 20; see also the Gulf of Mexico
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Representative terms from entire chapter:
nitrogen fertilizer
Colloquium Paper: Socolow
Hypoxia Assessment Plan at http://www.cop.noaa.gov/
HypoxiaPlan.html;~.
Nitrogen Addition to Ecosystems Reduces Biodiversity and
Thereby Leads to Loss of Ecosystem Function. Both by air and
water routes, fixed nitrogen deliberately applied to crops finds
its way to unmanaged ecosystems, leading to their inadvertent
fertilization. Schlesinger (21) writes: "Vegetation on much of
the Earth's land surface exists in a state of nitrogen deficiency,
due in part to the low natural rate of nitrogen fixation and
persistent losses of available nitrogen to denitrification and
nitrate leaching. . . We know from a large ecological literature
that~the fertilization of natural ecosystems, perhaps first noted
in the eutrophication of lakes, is likely to result in a loss of
species diversity. . . Any addition of a resource to ta natural
community where that resource is scarce] will lead to the
dominance of the species that can use that resource most
efficiently." Rather than having a net positive effect, inadver-
tent fertilization alters ecosystem composition and diminishes
ecosystem function (22-25~.
Lessons from Carbon and Energy for Nitrogen and Food
Efforts already underway to manage human impacts on the
carbon cycle suggest five principles that could guide first steps
to manage human impacts on the nitrogen cycle: (i) reach
agreement on goals relevant to sustainability; (
6006 Colloquium Paper: Socolow
fine-tuning the quantity applied to reflect soil variability (36~.
Smil (7) estimates that the "cumulative effect of adopting
well-proven and low-cost measures aimed at increasing effi-
ciency of nutrient uptake" would expand the effective global
supply of nitrogen fertilizer by about 20 Mt(N)/yr. About half
of the increment would come from improved fertilizer man-
agement and about half from reducing erosion, expanding the
use of nitrogen-fixing crops, and increasing the recycling of
organic wastes.
Animals. Of the many losses of fixed nitrogen in the animal
system, probably the most important are the losses associated
with the nitrogen in manure. Geographic separation of feed-
lots and dairies from sites of crop production, a relatively
recent phenomenon, has greatly raised the cost of recycling
animal wastes. Even though consolidation of livestock man-
agement into large commercial units reduces collection costs,
transportation costs make loop-closing uneconomic. With the
Netherlands in the lead, public policy is forcing new manage-
ment strategies for manure that are more responsive to envi-
ronment and public health.
As per-capita income rises in most countries, this ineffi-
ciency grows in importance, because an increasing fraction of
the flows of nitrogen from plants to people involves animals as
intermediaries. In recent years, 40% of global grain production
has gone to animal feed, but in the United States this fraction
is 70~o, and in Asia it has climbed in the last decade (1985-1987
versus 1995-1997) from 15% to 24% (37~. There is a parallel
in the energy system: as income rises, an increasing fraction of
fossil fuel energy reaches the consumer through the interme-
diary of electricity. Meat is the electricity of food.
Food consumption. There are losses of fixed nitrogen
throughout the food system: in the ships and trucks transport-
ing food, in the markets where it is sold, and in the kitchens and
restaurants where it is prepared. Neither the most important
losses nor the losses most easily reduced are easily identified.
Any analysis of nitrogen flows through the food system must
take cultural factors into account. "Culture . . . defines which
biological raw materials are seen as food and which are not"
(33~. For most of the world's people, eating is a form of
pleasure, enhanced by variety and free choice. In response,
agriculture becomes more varied and more international.
Overeating looms large.
How much nitrogen is required in food? The nutritionists'
recommended protein requirements (effectively, nitrogen re-
quirements) have dropped over time, as knowledge has im-
proved and as the ideal of a child growing as big as possible has
been recognized to be a cultural construct. Sasson (38) writes:
"It is not necessary to enjoy good health to have a diet where
proteins represents 15% or more of the total caloric intake. A
much lower proportion (5% in the case of good quality
proteins such as those in eggs or milk, or 8% in the case of other
types of proteins) is sufficient to cover the needs of an
individual, child or adult, as long as he has an adequate calorie
intake as well. Human milk contains only 5-6% of its energy
in the form of proteins and yet it is an ideal food for the
newborn child."
The global grain yield (60% of all food production) has had
almost the same nitrogen intensity (nitrogen percent by
weight) over the past three decades, because the rates of
growth of production of wheat, rice, and corn, each with its
distinct nitrogen intensity, have been almost identical, about
2.5% per year (39~. There appears to be no trend analogous to
the "decarbonization" of the energy economy, the continuous
decrease in the average carbon content of fuel throughout the
20th century that resulted from coal losing market share to
petroleum and then petroleum losing market share to natural
gas.
Harness Market Forces. A general message from theory and
experience is that market mechanisms are efficient. They
stimulate the collective imagination, which is inevitably more
Proc. Natl. Acad. Sci. USA 96 (1999J
powerful than the imagination of any small set of people who
try to discern constructive behaviors on their own. Market
mechanisms affect both producers and consumers. Market
mechanisms reward those who do more than they need to do,
relative to some yes-no measure of compliance. The "fertilizer
sector" has not heeded this message. Instead, it "has been
characterized by protection, subsidies, and price con-
trols" (40~.
Among the market mechanisms available for nitrogen man-
agement are cap-and-trade regimes, where a specified number
of permits to fix nitrogen are issued and traded (41~. Argu-
ments in favor of setting caps on fixed-nitrogen inputs to a
given region are beginning to be marshaled (42~. The permit
system could be organized at the watershed level, the national
level, or the international level. A cap-and-trade precedent at
the national level is the tradable permit system for atmospheric
sulfur dioxide emissions from U.S. coal-fired power plants.
The regime's first years have been unexpectedly successful
(43~. This particular trading system had features that enabled
it to survive a politically charged design process: it involved
only a small number of traders (on the order of 100), the
measurement of emissions was relatively straightforward, and
the political consensus that made enforcement credible was in
place. The U.S. has no cap-and-trade system for NOX emis-
sions, even though the principal motivation (reducing acid
precipitation) is the same. Beginning with trading in NOX
emissions is a sensible way to gain the experience necessary to
implement full-scale trading in fixed nitrogen.
Isn't more expensive food the inevitable consequence of
policy interventions to address previously ignored environ-
mental impacts of agriculture? And isn't more expensive food
a scourge on the poor? Experience in the energy sector
suggests two ways out of this trap. First, when priority is given
to new problems, new ideas emerge; tradeoffs turn into joint
gains. One learns to produce food more cheaply and with
reduced environmental consequences. Second, general subsi-
dies can be replaced by targeted subsidies for the poor. In the
regulated rate schedules for electricity, the first few units of
consumption (the first 100 kilowatt hours per month, for
example) often are subsidized. Such "lifeline rates," in both
industrialized and developing countries, are a clever mediator
between efficiency and equity, because the limited fraction of
total use by poor families makes the impact of lifeline rates
minimal (44~.
Incorporate Mechanisms to Learn Continuously from Re-
search. Crop physiology and ecophysiology have been identi-
fied as areas of agricultural science that hold the key to
substantial expansion of global food supply. Basic understand-
ing of the soil-crop interactions that govern yield in today's
most productive regions should permit greater "ecological
intensification," higher "input end-use efficiency" and better
protected "natural resource quality" (36~.
Basic understanding of soil-crop interactions also should
permit crops to be grown safely for the twin objectives of food
(or feed) and energy, a strategy of interest in both industrial-
ized and developing countries. The food component of a plant
and the residue would be managed jointly, informed by a
detailed understanding of how much residue should be re-
turned to the land. Wherever, in high-yield agriculture, the
soil's need for carbon could be satisfied by a fraction of the
total carbon in residues, the rest of the carbon in residues
would be freed for commercial use. Today's practice of burning
residues on the field could be replaced by high-technology
processing of residues for electricity and fuels (45~. And if
more of the nitrogen must be returned to the soil than would
come along with the residues recycled for carbon, then the
nitrogen and the carbon in the unrecycled residues might be
unbundled and managed separately, the nitrogen meeting the
needs at the field of origin, and, if some is left, serving as
fixed-nitrogen input elsewhere. The requirements of the soil
Colloquium Paper: Socolow Pro c. Natl. Acad. Sci. USA 96 (1999J 6007
for other nutrients and micronutrients also would have to be
met.
At the intersection of agricultural and environmental sci-
ence, the priority is to understand the transport and fate of
nitrogen nutrient, as well as the ecological consequences of
increased nitrogen input (24~. In nitrogen-cycle research there
is a "missing fixed-nitrogen problem" analogous to the "miss-
ing carbon" problem in global climate research: little is known
about the rate at which anthropogenic fixed nitrogen is deni-
trified in terrestrial and aquatic ecosystems (8~. The recent
result that terrestrial sinks for atmospheric carbon dioxide, per
unit area at the continent level, are larger than ecologists
expected (46) provides further reason to understand how
nutrient-enriched ecosystems evolve over time. If, for example,
50 Mt(N)/yr of today's anthropogenically fixed nitrogen
(about one-third of the total) were forming recalcitrant or-
ganic compounds at a C/N mass ratio of 20:1 (a molar ratio of
23:1), carbon would be sequestered in organic matter at a rate
of 1,000 Mt(C)/yr, one-sixth of the current rate of carbon
emissions from fossil fuels.
Economists and agronomists are locked in debate about
likely future yields. In the energy world, economists and
geologists are locked in virtually the same debate, this time
about likely additions to reserves of fossil fuels. The reason for
lack of resolution is the same. The historical record shows a run
of successes (higher yields, new reserves) for many decades.
Because the method of the economists is to predict future
outcomes from past performance, economists expect success
to continue. And because for the scientists future success
depends on discoveries they will have to make and do not now
know how to make, the scientists are doubtful. At its core, this
disagreement is about the pace of technical change. Agrono-
mists are the geologists of food.
Engage the Consumer and the Citizen. In the early 1970s the
previously separate concerns for energy production and en-
ergy use merged into a single inquiry. The oil field, the gasoline
station, the car engine, and alternatives to commuting to work
now were linked. The system was further enlarged by thinking
of the consumer not as someone who devours a certain amount
of energy but as someone who has to be provided a service or
amenity, such as transportation or lighting or a warm space. In
the case of the agriculture and food system such a merger
would integrate the perspectives of the agronomist and the
nutritionist, the farmer and the eater.
The protein consumption of large numbers of ever better fed
people dominates the impacts of food consumption on the
nitrogen cycle. Consider what the Food and Agriculture
Organization reports about the 110-g daily protein consump-
tion of the average American. Of the 40 g of vegetable protein,
25 are from grains, and 15 are from other sources. Of the 70 g
of animal protein, 40 are from meat, 20 from milk, five from
eggs, and five from fish and seafood (Food and Agriculture
Organization of the United Nations, http://apps.fao.org/
limS00/nph-wrap.pl?FoodBalanceSheet&Domain = Food
BalanceSheet). This diet is beckoning the rest of the world
(474. Food preferences, beliefs about healthy eating, social
norms, ethical constraints such as a concern for animal wel-
fare: these are among the factors that determine how our
eating disrupts the nitrogen cycle.
The individual is not only an eater but a citizen. Here energy
again is a guide, this time to political discourse. Desire for
autonomy drives interest in solar energy. Mistrust of expertise
fuels arguments against nuclear power. Organic farming is the
solar energy of food. Agricultural biotechnology is the nuclear
power of food.
Agricultural biotechnology is at risk of repeating the course
followed by nuclear power. Those in charge believe the way to
deal with the public's qualms is "to educate," but listening
would be more productive. The stakes are high. The develop-
ment of nitrogen-fixing corn and wheat, for example, could
transform nitrogen management, but with what other conse-
quences?
Questions burgeon: How well understood is the underlying
science, and how quickly is the science becoming better
known? Where are the irreversibilities? If scientists are the
guardians, who guards the guardians? And who protects all of
us from guardians of the guardians who see their task as
avoiding every potentially slippery slope, thereby annulling the
spirit of experimentation so critical to our future?
Conclusions
Through numerous feedback loops the impacts of agriculture
on the environment become impacts of agriculture on agri-
culture. Impacts on both the nitrogen and the carbon cycle
result in changes in climate, changes in soil characteristics,
changes in species mix, changes in pest populations, some of
which will benefit agriculture, but many of which will not.
Indeed, the existence of these closed loops is one of the
principal reasons why impacts of agriculture on the environ-
ment merit the attention of the agriculture community.
The finding that the nitrogen cycle at several spatial scales
is strongly impacted by food production should not surprise us.
Consistently, when one investigates the effects of aggregate
human activity on the natural world, one finds ecological
systems that are stressed by this activity. Consistently, one finds
that these stresses are only partially understood, that built-in
self-correcting mechanisms to keep these stresses from be-
coming dangerous are largely absent; that deliberate mitigat-
ing actions are not hard to find once the problem receives
sustained attention; and that at least some of the mitigating
actions that emerge from such an exercise are ethically com-
plex.
The societal response to the new knowledge that abundant
fixed nitrogen produces negative environmental effects has
been appropriately cautious. Nitrogen fertilizer, along with
improved seed and irrigation, are the "technological trinity"
responsible for the high-yield agriculture of the Green Revo-
lution (40~. High-yield agriculture, in turn, has been key to
avoiding mass starvation in much of the world. Poorly devised
strategies to reduce the use of fertilizer could lead, in the short
term, not only to human distress but also to environmental
adversity, were such efforts to result in production, on the
margin, from lands relatively vulnerable to environmental
damage (land on steep slopes, wetlands).
Nonetheless, it is inevitable that the agriculture and food
system will evolve to contain its impacts on biogeochemical
cycles. As rational policy regimes replace more opportunistic
ones, the agriculture and food system will be subject to the
same governance as other industrial systems (48, 49~. At the
level of the field, greater inputs of information and fewer
inputs of chemicals (including nitrogen fertilizer) are a likely
outcome.
Management of the nitrogen cycle can be informed by the
greater experience to date in managing the carbon cycle. There
are familiar objectives, uncertainties, environmental risks, and
collisions of values. Among the promising approaches are: (i)
setting a goal of ecosystem stabilization; (~ii) searching the
entire production and consumption system for opportunities to
improve efficiency; (~iii) implementing cap-and-trade systems
for fixed-nitrogen; (in) expanding research at the intersection
of agriculture and ecology, and (v) focusing on the food choices
of the prosperous.
Coordinated management of the nitrogen and carbon cycles
is required to address key environmental issues. The global
increase in fixed nitrogen may be fertilizing the Earth, trans-
ferring significant amounts of carbon from the atmosphere to
the biosphere, and mitigating global warming. A modern
biofuels industry someday may produce biofuels from crop
residues or dedicated energy crops, reducing the rate of fossil
6008 Colloquium Paper: Socolow
fuel use, while losses of nitrogen and other nutrients are
minimized. A basic research program that addresses the
critical scientific questions today limiting agricultural produc-
tivity is likely to address nitrogen fertilization and biomass
energy as well.
The agriculture and food community can be expected to
resist external pressure. However, the long-run consequence of
this pressure is likely to be beneficial. A new challenge
stimulates fresh approaches that result in greater efficiency,
here, in particular, in managing fixed nitrogen. Greater effi-
ciency will reduce both the external intrusion and the impact
on costs.
Among those who have tried to educate me about some of the
themes of this paper are Braden Allenby, Allison Armour-Garb, Jesse
Ausubel, Robert Ayres, Kenneth Cassman, James Galloway, Hiram
Levy, William Keene, Ann Kinzig, Emily Matthews, Jeremiah Os-
triker, Ted Parson, Jane Pitt, Vernon Ruttan, William Schlesinger,
Vaclav Smil, Christopher Taylor, Valerie Thomas, David Tilman, Iddo
Warnick, Bess Ward, and Robert Williams.
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