737
Ecological Applications,
7(3), 1997, pp. 737–750
q
1997 by the Ecological Society of America
HUMAN ALTERATION OF THE GLOBAL NITROGEN CYCLE:
SOURCES AND CONSEQUENCES
P
ETER
M. V
ITOUSEK
,
2
J
OHN
D. A
BER
,
3
R
OBERT
W. H
OWARTH
,
4
G
ENE
E. L
IKENS
,
5
P
AMELA
A. M
ATSON
,
6
D
AVID
W. S
CHINDLER
,
7
W
ILLIAM
H. S
CHLESINGER
,
8
AND
D
AVID
G. T
ILMAN
9
2
Department of Biological Sciences, Stanford University, Stanford, California 94305 USA
3
Complex Systems Center, University of New Hampshire, Durham, New Hampshire 03824 USA
4
Section of Ecology and Systematics, Cornell University, Ithaca, New York 14850 USA
5
Institute of Ecosystem Studies, Mary Flagler Cary Arboretum, Millbrook, New York 12545 USA
6
Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720 USA
7
Department of Biological Sciences, University of Alberta, Edmonton, Alberta Canada T6G 2E9
8
Department of Botany, Duke University, Durham, North Carolina 27709 USA
9
Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, Minnesota 55108 USA
Abstract.
Nitrogen is a key element controlling the species composition, diversity, dynamics, and functioning
of many terrestrial, freshwater, and marine ecosystems. Many of the original plant species living in these
ecosystems are adapted to, and function optimally in, soils and solutions with low levels of available nitrogen.
The growth and dynamics of herbivore populations, and ultimately those of their predators, also are affected
by N. Agriculture, combustion of fossil fuels, and other human activities have altered the global cycle of N
substantially, generally increasing both the availability and the mobility of N over large regions of Earth. The
mobility of N means that while most deliberate applications of N occur locally, their influence spreads regionally
and even globally. Moreover, many of the mobile forms of N themselves have environmental consequences.
Although most nitrogen inputs serve human needs such as agricultural production, their environmental conse-
quences are serious and long term.
Based on our review of available scientific evidence, we are certain that human alterations of the nitrogen
cycle have:
1) approximately doubled the rate of nitrogen input into the terrestrial nitrogen cycle, with these rates still
increasing;
2) increased concentrations of the potent greenhouse gas N
2
O globally, and increased concentrations of other
oxides of nitrogen that drive the formation of photochemical smog over large regions of Earth;
3) caused losses of soil nutrients, such as calcium and potassium, that are essential for the long-term
maintenance of soil fertility;
4) contributed substantially to the acidification of soils, streams, and lakes in several regions; and
5) greatly increased the transfer of nitrogen through rivers to estuaries and coastal oceans.
In addition, based on our review of available scientific evidence we are confident that human alterations of the
nitrogen cycle have:
6) increased the quantity of organic carbon stored within terrestrial ecosystems;
7) accelerated losses of biological diversity, especially losses of plants adapted to efficient use of nitrogen,
and losses of the animals and microorganisms that depend on them; and
8) caused changes in the composition and functioning of estuarine and nearshore ecosystems, and contributed
to long-term declines in coastal marine fisheries.
Manuscript received 1 November 1996. Reprints of this 14-page report are available for $2.25 each. Prepayment isrequired.
Order reprints from the Ecological Society of America, Attention: Reprint Department, 2010 Massachusetts Avenue, NW,
Suite 400, Washington, D.C. 20036.
738 PETER M. VITOUSEK ET AL.
Ecological Applications
Vol. 7, No. 3
Key words: agriculture and the global N cycle; anthropogenic global change; biological diversity
and the nitrogen cycle; ecosystem functioning, control by N; eutrophication of estuaries; global N-cycle
alteration, scientific consensus on; nitrogen-containing trace gases; nitrogen cycle, global; nitrogen
deposition and nitrogen loss; nitrogen and land–water interactions.
I
NTRODUCTION
The productivity and dynamics of many unmanaged
terrestrial and marine ecosystems, and most agricul-
tural and managed-forestry ecosystems, are limited by
the supply of biologically available nitrogen. Humans
are altering the global cycle of N via combustion of
fossil fuels, production of nitrogen fertilizers, culti-
vation of nitrogen-fixing legumes, and other actions
(Galloway et al. 1995). Increased N availability in-
creases productivity and biomass accumulation sub-
stantially, at least in the short-term (Vitousek and Ho-
warth 1991). Consequently, changes in N can alter the
global cycle of C, affecting both the rate of increase
of carbon dioxide in the atmosphere and the response
of ecosystems to that increase (Schimel et al. 1995).
Increasing N availability also generally reduces the bi-
ological diversity of affected ecosystems, and changes
the rates and pathways of N cycling and loss (Tilman
1987, Berendse et al. 1993, Aber et al. 1995). Nitrate
leaches through soils to stream water and groundwater,
depleting soil minerals, acidifying soils, and altering
downstream freshwater and coastal marine ecosystems
(Likens et al. 1996, Nixon et al 1996); reactive oxides
of N are important precursors of both acid rain and
photochemical smog, and can be transported hundreds
of kilometers to downwind ecosystems (Chameides et
al. 1994); long-lived nitrous oxide contributes to an-
thropogenic enhancement of the greenhouse effect (Al-
britton et al. 1995). This report reviews and summarizes
the extent of human alteration of the N cycle, and con-
sequences for the functioning of terrestrial, freshwater,
and marine ecosystems. It is not an exhaustive com-
pilation of such studies—that would require volumes.
Rather, it presents an overview of the current state of
scientific understanding of this human-caused global
change.
H
UMAN
A
LTERATION OF THE
G
LOBAL
NC
YCLE
The cycle of N is unique in that it consists of a
massive, well-mixed, and (to most organisms) wholly
unavailable pool of nitrogen gas (N
2
) in the atmo-
sphere; a relatively small and almost wholly biologi-
cally mediated conversion of N
2
to chemical forms of
N that are available to most organisms; and a pool of
N that cycles among plants, animals, microorganisms,
soils, solutions, and sediments, and between land, wa-
ter, and the atmosphere (Delwiche 1970). The most
fundamental human-caused change to the global N cy-
cle is a doubling of the transfer from the vast and un-
reactive atmospheric pool to biologically available
forms on land (termed ‘‘N fixation’’).
As with any other human-caused global change, it
is necessary to evaluate the state of the N cycle prior
to extensive human alteration, as well as the magnitude
of current human effects upon the cycle. And as with
many global changes, determining the background state
of the N cycle is difficult. Two natural processes trans-
fer N from N
2
to biologically available forms—light-
ning and biological N fixation. The latter is carried out
by microorganisms, many of them in symbiotic rela-
tionships with higher plants (especially legumes) and
algae. In analyzing the global N cycle, the standard
unit of measure is the teragram (10
12
g, abbreviated
Tg), or million (10
6
) metric tons of N. Lightning fixes
,
10 Tg N/yr now (Galloway et al 1995), and it has
not been affected by human activity. Estimates of bi-
ological N fixation in marine ecosystems are variable
and uncertain, ranging from
,
30 Tg/yr to
.
300 Tg/yr
(Carpenter and Capone 1983, Carpenter and Romans
1991, Galloway et al 1995). Estimates of nitrogen fix-
ation in terrestial ecosystems are better constrained;
prior to extensive human activity, organisms probably
fixed between 90 and 140 Tg N/yr (Soderlund and Ross-
wall 1982, Paul and Clark 1989, Schlesinger 1991).
Several recent reviews demonstrate that human activity
clearly has enhanced rates of N fixation on land sub-
stantially (Fig. 1) (Smil 1990, 1991, Vitousek and Mat-
son 1993, Ayers et al 1994, Galloway et al 1995). A
number of pathways are involved, including industrial
fixation of N
2
for use as fertilizer, cultivation of crops
with the capacity to fix N symbiotically, and mobili-
zation and fixation during fossil-fuel combustion.
Sources of change
N fertilizer.
—Current industrial fixation of N for use
as fertilizer totals
ø
80 Tg/yr (FAO 1993). This figure
does not include manures and other organic N fertil-
izers; globally, these account for more N than does
industrial fertilizer, but manure application represents
recycling of already-fixed N rather than new fixation.
Industrial N fixation has increased exponentially from
near zero in the 1940s. Until the late 1970s, most in-
dustrial N fertilizer was applied in developed countries,
but use there has stabilized while applications in de-
veloping countries have increased dramatically. The
immediacy and rapidity of the recent increase in N
fixation is difficult to overstate. For example, Kates et
al. (1990) point out more than half of all the industrially
fixed N applied in human history up to 1990 had been
used since 1980 (Fig. 2). The momentum of human
population growth and increasing urbanization ensure
that industrial N fixation will continue at high rates for
decades.
Fossil fuel combustion.
—The burning of fossil fuels
August 1997 739
ALTERATION OF THE GLOBAL N CYCLE
F
IG
. 1. Anthropogenic fixation of N in terrestrial ecosys-
tems over time, in comparison with the range of estimates of
natural biological N fixation on land. Modified from Galloway
et al. (1995: Fig. 5).
F
IG
. 2. Comparative timing of a number of global
changes. Considering the extent of change as of the late 1980s
as 100%, the figure shows the year by which 25%, 50%, and
75% of the overall change in deforestation, CO
2
release to
the atmosphere, human population growth, and application
of industrial fertilizer N had occurred. Revised from Kates
et al. (1990:Fig. 1.1).
transfers fixed N from long-term geological reservoirs
to the atmosphere, and high-temperature combustion
fixes a small amount of atmospheric N
2
. A total of
.
20
Tg/yr of fixed N is emitted to the atmosphere during
fossil-fuel combustion.
Nitrogen-fixing crops.
—Leguminous crops and for-
ages (i.e., soybeans, peas, alfalfa) support symbiotic
N-fixing microorganisms, and thereby derive much of
their N directly from atmospheric N
2
. Fixation of N in
excess of background rates in the natural communities
that legume crops have replaced represents new, an-
thropogenic N fixation. There is also substantial bio-
logical N fixation associated with cultivation of some
non-legumes, notably rice. The quantity of N fixed by
crops is more difficult to determine than is industrial
N fixation; Galloway et al. (1995) estimate it at 32–53
Tg/yr, and we will use 40 Tg/yr as an estimate here.
Mobilization of N.
—In addition to enhancing fixa-
tion, human activity liberates N from long-term bio-
logical storage pools, and thereby contributes further
to increasing the biological availability of N. The major
pathways of mobilization are discussed in Vitousek and
Matson (1993); they include biomass burning, which
volatilizes
.
40 Tg/yr of N, with
ø
20 Tg/yr of that
fixed N (Lobert et al. 1990, Andreae 1993); land clear-
ing and conversion, which could mobilize 20 Tg/yr;
and the drainage of wetlands and consequent oxidation
of their organic soils, which could mobilize 10 Tg/yr
or more (Armentano 1980). Moreover, the loss of wet-
lands removes a significant sink for fixed nitrogen (de-
nitrification, the conversion of nitrate to N
2
under an-
aerobic conditions), further increasing the mobility of
N to and through streams and rivers (Leonardson 1994).
All of these pathways have substantial uncertainties in
both the quantity of N mobilized and its fate, but to-
gether they could contribute significantly to increasing
the biological availability of N.
Overall, human activity causes the fixation of
ø
140
Tg of new N per year in terrestrial ecosystems (Fig.
1)—at the upper end of the range of estimates for total
background N fixation on land—and mobilizes perhaps
70 Tg more. It is fair to conclude that human activity
has doubled (or more) the transfer of N from the at-
mosphere to biologically available pools on land. The
added N is spread unevenly over Earth’s surface—some
areas (e.g., northern Europe) are profoundly altered
(Berendse et al. 1993, Wright and van Breeman 1995),
while others (e.g., remote south-temperate regions) re-
ceive little direct input (Galloway et al. 1982, Hedin
et al. 1995)—but no place on Earth is unaffected. The
recent increase in the quantity of fixed N in circulation
is readily detectable in cores from the glacial ice of
Greenland (Mayewski et al. 1986).
E
FFECTS ON THE
A
TMOSPHERE
The modern increase in fixation and mobilization of
nitrogen is associated with increased emission, trans-
port, reaction, and deposition of trace nitrogen gases,
including nitrous oxide (N
2
O), nitric oxide (NO), and
ammonia (NH
3
). Some human activities affect the at-
mosphere directly; for example, essentially all of the
.
20 Tg of N fixed or mobilized during fossil-fuel com-
bustion and other high-temperature processes is emit-
ted to the atmosphere as NO. Human activities also
increase emissions indirectly. For example, agricultural
fertilization increases the concentration of volatile NH
3
in soils, increases microbial processing of fixed N, and
ultimately increases emissions of nitrogen gases from
soils and groundwater (Eichner 1990, Schlesinger and
Hartley 1992). Similarly, inadvertent N fertilization of
unmanaged ecosystems downwind of agricultural/in-
dustrial areas can increase gas emissions from their
soils.
These anthropogenic changes in the nitrogen cycle
drive regional and global changes in the atmosphere.
Nitrous oxide is increasing at the rate of 0.2–0.3%/yr,
with most of the change occurring recently (Prinn et
al. 1990). Nitrous oxide is a very effective greenhouse
740 PETER M. VITOUSEK ET AL.
Ecological Applications
Vol. 7, No. 3
F
IG
. 3. The anthropogenic contribution to the total emis-
sions of nitrogen-containing trace gases. Ammonia data are
from Schlesinger and Hartley (1992), nitric oxide from Del-
mas et al. (
in press
), and nitrous oxide from Prather et al.
(1995).
gas that absorbs infrared radiation in spectral windows
not covered by other gases; it contributes a few percent
to overall greenhouse warming (Albritton et al. 1995).
It is unreactive in the troposphere, but it is destroyed
by photolysis or by reaction with excited oxygen atoms
in the stratosphere, where it can catalyze the destruction
of stratospheric ozone (Crutzen and Ehhalt 1977).
While the increasing concentration of N
2
O is clearly
documented, the sources of that increase remain a mat-
ter of some discussion. Both fossil-fuel combustion and
direct consequences of agricultural fertilization have
been considered and rejected as the major source; there
is a developing consensus that many anthropogenic
sources (fertilizers, N-enriched groundwater, N-satur-
ated forests, biomass burning, land clearing, nylon
manufacture) all contribute to the increase (Prather et
al. 1995). This ‘‘dispersed source’’ view is consistent
with a terrestrial N cycle that has been systematically
enriched by anthropogenic N fixation (Fig. 1).
In contrast to N
2
O, NO and NH
3
are highly reactive
in the atmosphere, and changes in their concentrations
must be evaluated on local, regional, or subcontinental
scales. Nitric oxide plays several critical roles in at-
mospheric chemistry. It affects the concentration of the
main oxidizing agent in the atmosphere, the hydroxyl
(OH) radical (Logan 1985). Moreover, it contributes
(often in a rate-limiting way) to the photochemical for-
mation of tropospheric ozone (O
3
), the most important
atmospheric gaseous pollutant in terms of its effects
on human health and plant productivity (Reich and
Amundson 1985, Chameides et al. 1994). When NO
concentrations are high, the oxidation of carbon mon-
oxide (CO), non-methane hydrocarbons, and methane
(CH
4
) leads to a net production of tropospheric ozone
(Jacob and Wofsy 1990, Williams et al 1992); when
NO concentrations are low, oxidation of these com-
pounds is a sink for ozone. Finally, the end product of
NO oxidation, nitric acid, is a principal component of
acid rain. As with N
2
O, a number of sources contribute
to NO emissions, including microbial activity in fer-
tilized soils. However, combustion is the dominant
source; fossil fuel combustion emits
.
20 Tg/yr, and
biomass burning (now mostly human-caused) may add
about 8 Tg/yr more (Levy et al. 1991). Global NO
emissions from soils total 5–20 Tg/yr (Yienger and
Levy 1994, Davidson 1991) and a substantial fraction
of this N is anthropogenic. Overall, 80% or more of
all NO emissions globally are human-caused (Fig. 3;
Delmas et al.,
in press
).
Ammonia (NH
3
) is the primary acid-neutralizing
agent in the atmosphere, where it influences the pH of
aerosols, cloudwater, and rainfall. As with NO, NH
3
emissions from ecosystems, transport in the atmo-
sphere, and return to ecosystems via gas absorption,
dry deposition, or in solution represent important path-
ways of nitrogen movement between ecosystems. Nu-
merous studies have demonstrated substantial volatil-
ization of fertilizer N as NH
3
(Fenn and Hossner 1985,
Denmead 1990); Schlesinger and Hartley (1992) esti-
mate NH
3
-N fluxes from fertilized fields at 10 Tg/yr.
Emissions from domestic animal wastes (32 Tg/yr) and
biomass burning (5 Tg/yr) are also important globally;
in sum, anthropogenic sources account for nearly 70%
of all global ammonia emissions (Schlesinger and Hart-
ley 1992; Fig. 3).
Enhanced emissions of N to the atmosphere have led
to enhanced deposition of N on land and in the oceans.
Based on extensive measurements of precipitation in
remote areas of the southern hemisphere, where an-
thropogenic deposition of N is minimal, annual wet
deposition of inorganic N in unpolluted regions aver-
ages 0.1–0.7 kg N/ha, of which 40% is nitrate and 60%
is ammonium (Galloway et al. 1982, 1996, Likens et
al. 1987). These fluxes are
,
10% of rates of wet de-
position in the human-altered midwestern and eastern
United States and
,
1% of rates in the most heavily
affected areas of northern Europe (Berendse et al. 1993,
Wright and Van Breeman 1995).
E
FFECTS ON
T
ERRESTRIAL
E
COSYSTEMS
N enrichment and the C cycle
It is clear that rates of plant production and of the
accumulation of biomass in whole ecosystems are lim-
ited by N supply over much of Earth’s surface (Tamm
1991, Vitousek and Howarth 1991), particularly in tem-
perate and boreal regions, and equally clear that human
activity has increased N deposition substantially over
much of this area. How much C is stored within ter-
restrial ecosystems as a consequence of anthropogenic
N fixation and deposition? This question has important
implications for the global cycle of C, in that deposition
of anthropogenic fixed N could help to explain the
‘‘missing sink,’’ the imbalance between known CO
2
August 1997 741
ALTERATION OF THE GLOBAL N CYCLE
emissions from fossil fuel combustion and deforesta-
tion vs. known CO
2
accumulation in the atmosphere
(Schimel et al. 1995).
Experimental work at European and American sites
indicates that a large portion of the nitrogen retained
by forest, wetland, and tundra ecosystems stimulates
carbon uptake and storage (e.g., Rasmussen et al. 1993,
Aber et al. 1995). Nitrogen deposition can also stim-
ulate decomposition in some forests (Boxman et al.
1995), but the effects of added N in stimulating pro-
duction are generally quantitatively more important
(Hunt et al. 1988, Berg and Tamm 1991).
A number of analyses have calculated how much
terrestrial C storage could result from N deposition
(Peterson and Melillo 1985, Schindler and Bayley
1993, Hudson et al. 1994, Townsend et al. 1996); es-
timates of net C storage range from 0.1 to 1.3 Pg C/yr
(1 Pg
5
1000 Tg). The magnitude of potential C storage
has tended to increase in more recent analyses, as the
magnitude of change in the global N cycle is better
appreciated (Keeling et al. 1996). The most recent anal-
ysis of the global C cycle by the Intergovernmental
Panel on Climate Change (IPCC) concluded that N de-
position could represent a major component of the
missing C sink (Schimel et al. 1995). Further refine-
ments could come from more complete analyses of the
fraction of anthropogenic
N
that is retained within ter-
restrial ecosystems, on regional to continental scales
(Galloway et al. 1995, Howarth et al. 1996).
Nitrogen saturation and ecosystem function
Ultimately, there are declining returns in the re-
sponse of plant production and carbon storage to ad-
ditions of N, and consequently the potential for eco-
systems to retain added N through increased production
and organic matter storage is limited. The term ‘‘ni-
trogen saturation’’ (A
˚
gren and Bosatta 1988, Aber et
al. 1989, Aber 1992) has been applied to changes in N
cycling in forest ecosystems that occur as N limitations
to biological functions are relieved by N additions. In
a fully N-saturated system (particularly one that is not
storing C for some other reason such as its stage of
stand development, or increasing CO
2
), N losses to
streams, groundwater, and the atmosphere should ap-
proach total N deposition, and any fertilization effects
or continued C storage should disappear.
Concerns regarding the effects of N deposition on
forest health and downstream ecosystems arose follow-
ing observation of significant increases in nitrate con-
centrations in some lakes and streams (Grennfelt and
Hultberg 1986, Henriksen and Brakke 1988, Stoddard
1994), and documented declines and mortality in co-
niferous evergreen forests in Europe (Schulze 1989).
These observations have led to several field experi-
ments that examined interactions between N deposition
and forest ecosystem function (e.g., Van Miegrot et al.
1992, Kahl et al. 1993, Wright and van Breeman 1995,
Magill et al. 1997). These experiments showed that
where increased N additions led to increased nitrate
mobility, the nitrate losses also led to losses of nutrient
cations and increases in soil and water acidity (Mc-
Nulty and Aber 1993, Boxman et al. 1995, Emmett et
al. 1995).
Excess N availability also can cause nutrient imbal-
ances in trees. These are expressed as root or foliar
element ratios, especially Ca:Al and Mg:N ratios. As
described below, Ca and Mg are lost via leaching, while
the availability of Al is enhanced by acidity. Such im-
balances may be linked to reductions in net photosyn-
thesis, photosynthetic N-use efficiency, forest growth,
and even increased tree mortality (Shortle and Smith
1988, Schulze 1989, Aber et al. 1995, Cronan and Gri-
gal 1995).
In the northeastern United States, large shifts in fo-
liar element ratios and increases in nitrate-leaching
losses are generally restricted to high-elevation sites
(which receive greater N deposition), those with shal-
low soils, those which have received little human dis-
turbance (which presumably were close to input–output
balance prior to receiving enhanced N deposition), and
those receiving experimental additions of N well above
ambient levels (e.g., Driscoll et al. 1987, Murdoch and
Stoddard 1991, Kahl et al. 1993). In contrast, forests
that have been subjected to intense or repeated biomass
removals have very high capacities to retain N (Aber
et al. 1995, Magill et al. 1997). The early stages of N
saturation have also been noted in response to elevated
N deposition in dry conifer forests surrounding the Los
Angeles Basin, California (Bytnerowicz and Fenn
1996), in the Front Range of the Colorado Rockies
(Baron et al. 1994), and in forests in which symbiotic
N-fixing organisms are major components (Van Mie-
groet 1992). Nitrogen saturation is much further ad-
vanced over extensive areas of northern Europe, where
rates of anthropogenic N deposition are several-fold
greater than the most extreme areas in North America
(Berendse et al. 1993).
Overall, the ability of a forest ecosystem to retain N
is linked to its productive potential, and the degree to
which previous disturbances have resulted in N re-
moval and current N limitations. Thus, the extent and
importance of N saturation are tightly linked to changes
in land use, climate, atmospheric CO
2
and O
3
, and other
environmental variables that are also subject to rapid
change.
Nitrogen deposition and changes in ecosystem
composition and biodiversity
The addition of limiting nutrients can dramatically
change which species are dominant in ecosystems and
markedly decrease the overall biodiversity of ecosys-
tems. For example, experimental additions of nitrogen
to grassland ecosystems in England have led to in-
creased dominance by a few nitrogen-demanding grass
![FIG. 4. Export of total nitrogen (a) and nitrate (b) from river systems, as a function of human population density in the watershed. Reprinted from Howarth et al. (1996:Fig. 3a, b) with permission of Kluwer Academic Publishers (where Fig. 3b was modified from Peierls et al. [1991]). Note logarithmic scale.](/figures/fig-4-export-of-total-nitrogen-a-and-nitrate-b-from-river-c55cff8v.webp)
