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
PETER M. VITOUSEK,2 JOHN D. ABER,3 ROBERT W. HOWARTH,4 GENE E. LIKENS,5 PAMELA A. MATSON,6
DAVID W. SCHINDLER,7 WILLIAM H. SCHLESINGER,8 AND DAVID G. TILMAN9
2Department of Biological Sciences, Stanford University, Stanford, California 94305 USA
3Complex Systems Center, University of New Hampshire, Durham, New Hampshire 03824 USA
4Section of Ecology and Systematics, Cornell University, Ithaca, New York 14850 USA
5Institute of Ecosystem Studies, Mary Flagler Cary Arboretum, Millbrook, New York 12545 USA
6Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720 USA
7Department of Biological Sciences, University of Alberta, Edmonton, Alberta Canada T6G 2E9
8Department of Botany, Duke University, Durham, North Carolina 27709 USA
9Department 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 N2O 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.
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738 PETER M. VITOUSEK ET AL. Ecological ApplicationsVol. 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.
INTRODUCTION is necessary to evaluate the state of the N cycle prior
The productivity and dynamics of many unmanaged to extensive human alteration, as well as the magnitude
terrestrial and marine ecosystems, and most agricul- of current human effects upon the cycle. And as with
tural and managed-forestry ecosystems, are limited by many global changes, determining the background state
the supply of biologically available nitrogen. Humans of the N cycle is difficult. Two natural processes trans-
are altering the global cycle of N via combustion of fer N from N2 to biologically available forms—light-
fossil fuels, production of nitrogen fertilizers, culti- ning and biological N fixation. The latter is carried out
vation of nitrogen-fixing legumes, and other actions by microorganisms, many of them in symbiotic rela-
(Galloway et al. 1995). Increased N availability in- tionships with higher plants (especially legumes) and
creases productivity and biomass accumulation sub- algae. In analyzing the global N cycle, the standard
12
stantially, at least in the short-term (Vitousek and Ho- unit of measure is the teragram (10 g, abbreviated
warth 1991). Consequently, changes in N can alter the Tg), or million (10
6) metric tons of N. Lightning fixes
global cycle of C, affecting both the rate of increase ,10 Tg N/yr now (Galloway et al 1995), and it has
of carbon dioxide in the atmosphere and the response not been affected by human activity. Estimates of bi-
of ecosystems to that increase (Schimel et al. 1995). ological N fixation in marine ecosystems are variable
Increasing N availability also generally reduces the bi- and uncertain, ranging from ,30 Tg/yr to .300 Tg/yr
ological diversity of affected ecosystems, and changes (Carpenter and Capone 1983, Carpenter and Romans
the rates and pathways of N cycling and loss (Tilman 1991, Galloway et al 1995). Estimates of nitrogen fix-
1987, Berendse et al. 1993, Aber et al. 1995). Nitrate ation in terrestial ecosystems are better constrained;
leaches through soils to stream water and groundwater, prior to extensive human activity, organisms probably
depleting soil minerals, acidifying soils, and altering fixed between 90 and 140 Tg N/yr (Soderlund and Ross-
downstream freshwater and coastal marine ecosystems wall 1982, Paul and Clark 1989, Schlesinger 1991).
(Likens et al. 1996, Nixon et al 1996); reactive oxides Several recent reviews demonstrate that human activity
of N are important precursors of both acid rain and clearly has enhanced rates of N fixation on land sub-
photochemical smog, and can be transported hundreds stantially (Fig. 1) (Smil 1990, 1991, Vitousek and Mat-
of kilometers to downwind ecosystems (Chameides et son 1993, Ayers et al 1994, Galloway et al 1995). A
al. 1994); long-lived nitrous oxide contributes to an- number of pathways are involved, including industrial
thropogenic enhancement of the greenhouse effect (Al- fixation of N2 for use as fertilizer, cultivation of crops
britton et al. 1995). This report reviews and summarizes with the capacity to fix N symbiotically, and mobili-
the extent of human alteration of the N cycle, and con- zation and fixation during fossil-fuel combustion.
sequences for the functioning of terrestrial, freshwater,
Sources of change
and marine ecosystems. It is not an exhaustive com-
pilation of such studies—that would require volumes. N fertilizer.—Current industrial fixation of N for use
Rather, it presents an overview of the current state of as fertilizer totals ø80 Tg/yr (FAO 1993). This figure
scientific understanding of this human-caused global does not include manures and other organic N fertil-
change. izers; globally, these account for more N than does
industrial fertilizer, but manure application represents
HUMAN ALTERATION OF THE GLOBAL N CYCLE recycling of already-fixed N rather than new fixation.
The cycle of N is unique in that it consists of a Industrial N fixation has increased exponentially from
massive, well-mixed, and (to most organisms) wholly near zero in the 1940s. Until the late 1970s, most in-
unavailable pool of nitrogen gas (N2) in the atmo- dustrial N fertilizer was applied in developed countries,
sphere; a relatively small and almost wholly biologi- but use there has stabilized while applications in de-
cally mediated conversion of N2 to chemical forms of veloping countries have increased dramatically. The
N that are available to most organisms; and a pool of immediacy and rapidity of the recent increase in N
N that cycles among plants, animals, microorganisms, fixation is difficult to overstate. For example, Kates et
soils, solutions, and sediments, and between land, wa- al. (1990) point out more than half of all the industrially
ter, and the atmosphere (Delwiche 1970). The most fixed N applied in human history up to 1990 had been
fundamental human-caused change to the global N cy- used since 1980 (Fig. 2). The momentum of human
cle is a doubling of the transfer from the vast and un- population growth and increasing urbanization ensure
reactive atmospheric pool to biologically available that industrial N fixation will continue at high rates for
forms on land (termed ‘‘N fixation’’). decades.
As with any other human-caused global change, it Fossil fuel combustion.—The burning of fossil fuels
August 1997 ALTERATION OF THE GLOBAL N CYCLE 739
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).
FIG. 1. Anthropogenic fixation of N in terrestrial ecosys-
tems over time, in comparison with the range of estimates of EFFECTS ON THE ATMOSPHERE
natural biological N fixation on land. Modified from Galloway
et al. (1995: Fig. 5). The modern increase in fixation and mobilization of
nitrogen is associated with increased emission, trans-
transfers fixed N from long-term geological reservoirs port, reaction, and deposition of trace nitrogen gases,
to the atmosphere, and high-temperature combustion including nitrous oxide (N2O), nitric oxide (NO), and
fixes a small amount of atmospheric N . A total of .20 ammonia (NH3). Some human activities affect the at-2
Tg/yr of fixed N is emitted to the atmosphere during mosphere directly; for example, essentially all of the
fossil-fuel combustion. .20 Tg of N fixed or mobilized during fossil-fuel com-
Nitrogen-fixing crops.—Leguminous crops and for- bustion and other high-temperature processes is emit-
ages (i.e., soybeans, peas, alfalfa) support symbiotic ted to the atmosphere as NO. Human activities also
N-fixing microorganisms, and thereby derive much of increase emissions indirectly. For example, agricultural
their N directly from atmospheric N2. Fixation of N in fertilization increases the concentration of volatile NH3
excess of background rates in the natural communities in soils, increases microbial processing of fixed N, and
that legume crops have replaced represents new, an- ultimately increases emissions of nitrogen gases from
thropogenic N fixation. There is also substantial bio- soils and groundwater (Eichner 1990, Schlesinger and
logical N fixation associated with cultivation of some Hartley 1992). Similarly, inadvertent N fertilization of
non-legumes, notably rice. The quantity of N fixed by unmanaged ecosystems downwind of agricultural/in-
crops is more difficult to determine than is industrial dustrial areas can increase gas emissions from their
N fixation; Galloway et al. (1995) estimate it at 32–53 soils.
Tg/yr, and we will use 40 Tg/yr as an estimate here. These anthropogenic changes in the nitrogen cycle
Mobilization of N.—In addition to enhancing fixa- drive regional and global changes in the atmosphere.
tion, human activity liberates N from long-term bio- Nitrous oxide is increasing at the rate of 0.2–0.3%/yr,
logical storage pools, and thereby contributes further with most of the change occurring recently (Prinn et
to increasing the biological availability of N. The major al. 1990). Nitrous oxide is a very effective greenhouse
pathways of mobilization are discussed in Vitousek and
Matson (1993); they include biomass burning, which
volatilizes .40 Tg/yr of N, with ø20 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 N2 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 FIG. 2. Comparative timing of a number of global
the biological availability of N. changes. Considering the extent of change as of the late 1980s
Overall, human activity causes the fixation of ø140 as 100%, the figure shows the year by which 25%, 50%, and
Tg of new N per year in terrestrial ecosystems (Fig. 75% of the overall change in deforestation, CO2 release tothe atmosphere, human population growth, and application
1)—at the upper end of the range of estimates for total of industrial fertilizer N had occurred. Revised from Kates
background N fixation on land—and mobilizes perhaps et al. (1990:Fig. 1.1).
740 PETER M. VITOUSEK ET AL. Ecological ApplicationsVol. 7, No. 3
pounds is a sink for ozone. Finally, the end product of
NO oxidation, nitric acid, is a principal component of
acid rain. As with N2O, 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 (NH3) is the primary acid-neutralizing
agent in the atmosphere, where it influences the pH of
aerosols, cloudwater, and rainfall. As with NO, NH3
FIG. 3. The anthropogenic contribution to the total emis- emissions from ecosystems, transport in the atmo-
sions of nitrogen-containing trace gases. Ammonia data are
from Schlesinger and Hartley (1992), nitric oxide from Del- sphere, and return to ecosystems via gas absorption,
mas et al. (in press), and nitrous oxide from Prather et al. dry deposition, or in solution represent important path-
(1995). ways of nitrogen movement between ecosystems. Nu-
merous studies have demonstrated substantial volatil-
gas that absorbs infrared radiation in spectral windows ization of fertilizer N as NH3 (Fenn and Hossner 1985,
not covered by other gases; it contributes a few percent Denmead 1990); Schlesinger and Hartley (1992) esti-
to overall greenhouse warming (Albritton et al. 1995). mate NH3-N fluxes from fertilized fields at 10 Tg/yr.
It is unreactive in the troposphere, but it is destroyed Emissions from domestic animal wastes (32 Tg/yr) and
by photolysis or by reaction with excited oxygen atoms biomass burning (5 Tg/yr) are also important globally;
in the stratosphere, where it can catalyze the destruction in sum, anthropogenic sources account for nearly 70%
of stratospheric ozone (Crutzen and Ehhalt 1977). of all global ammonia emissions (Schlesinger and Hart-
While the increasing concentration of N O is clearly ley 1992; Fig. 3).2
documented, the sources of that increase remain a mat- Enhanced emissions of N to the atmosphere have led
ter of some discussion. Both fossil-fuel combustion and to enhanced deposition of N on land and in the oceans.
direct consequences of agricultural fertilization have Based on extensive measurements of precipitation in
been considered and rejected as the major source; there remote areas of the southern hemisphere, where an-
is a developing consensus that many anthropogenic thropogenic deposition of N is minimal, annual wet
sources (fertilizers, N-enriched groundwater, N-satur- deposition of inorganic N in unpolluted regions aver-
ated forests, biomass burning, land clearing, nylon ages 0.1–0.7 kg N/ha, of which 40% is nitrate and 60%
manufacture) all contribute to the increase (Prather et is ammonium (Galloway et al. 1982, 1996, Likens et
al. 1995). This ‘‘dispersed source’’ view is consistent al. 1987). These fluxes are ,10% of rates of wet de-
with a terrestrial N cycle that has been systematically position in the human-altered midwestern and eastern
enriched by anthropogenic N fixation (Fig. 1). United States and ,1% of rates in the most heavily
In contrast to N O, NO and NH are highly reactive affected areas of northern Europe (Berendse et al. 1993,2 3
in the atmosphere, and changes in their concentrations Wright and Van Breeman 1995).
must be evaluated on local, regional, or subcontinental EFFECTS ON TERRESTRIAL ECOSYSTEMS
scales. Nitric oxide plays several critical roles in at-
mospheric chemistry. It affects the concentration of the N enrichment and the C cycle
main oxidizing agent in the atmosphere, the hydroxyl It is clear that rates of plant production and of the
(OH) radical (Logan 1985). Moreover, it contributes accumulation of biomass in whole ecosystems are lim-
(often in a rate-limiting way) to the photochemical for- ited by N supply over much of Earth’s surface (Tamm
mation of tropospheric ozone (O3), the most important 1991, Vitousek and Howarth 1991), particularly in tem-
atmospheric gaseous pollutant in terms of its effects perate and boreal regions, and equally clear that human
on human health and plant productivity (Reich and activity has increased N deposition substantially over
Amundson 1985, Chameides et al. 1994). When NO much of this area. How much C is stored within ter-
concentrations are high, the oxidation of carbon mon- restrial ecosystems as a consequence of anthropogenic
oxide (CO), non-methane hydrocarbons, and methane N fixation and deposition? This question has important
(CH4) leads to a net production of tropospheric ozone implications for the global cycle of C, in that deposition
(Jacob and Wofsy 1990, Williams et al 1992); when of anthropogenic fixed N could help to explain the
NO concentrations are low, oxidation of these com- ‘‘missing sink,’’ the imbalance between known CO2
August 1997 ALTERATION OF THE GLOBAL N CYCLE 741
emissions from fossil fuel combustion and deforesta- Magill et al. 1997). These experiments showed that
tion vs. known CO2 accumulation in the atmosphere where increased N additions led to increased nitrate
(Schimel et al. 1995). mobility, the nitrate losses also led to losses of nutrient
Experimental work at European and American sites cations and increases in soil and water acidity (Mc-
indicates that a large portion of the nitrogen retained Nulty and Aber 1993, Boxman et al. 1995, Emmett et
by forest, wetland, and tundra ecosystems stimulates al. 1995).
carbon uptake and storage (e.g., Rasmussen et al. 1993, Excess N availability also can cause nutrient imbal-
Aber et al. 1995). Nitrogen deposition can also stim- ances in trees. These are expressed as root or foliar
ulate decomposition in some forests (Boxman et al. element ratios, especially Ca:Al and Mg:N ratios. As
1995), but the effects of added N in stimulating pro- described below, Ca and Mg are lost via leaching, while
duction are generally quantitatively more important the availability of Al is enhanced by acidity. Such im-
(Hunt et al. 1988, Berg and Tamm 1991). balances may be linked to reductions in net photosyn-
A number of analyses have calculated how much thesis, photosynthetic N-use efficiency, forest growth,
terrestrial C storage could result from N deposition and even increased tree mortality (Shortle and Smith
(Peterson and Melillo 1985, Schindler and Bayley 1988, Schulze 1989, Aber et al. 1995, Cronan and Gri-
1993, Hudson et al. 1994, Townsend et al. 1996); es- gal 1995).
timates of net C storage range from 0.1 to 1.3 Pg C/yr In the northeastern United States, large shifts in fo-
(1 Pg 5 1000 Tg). The magnitude of potential C storage liar element ratios and increases in nitrate-leaching
has tended to increase in more recent analyses, as the losses are generally restricted to high-elevation sites
magnitude of change in the global N cycle is better (which receive greater N deposition), those with shal-
appreciated (Keeling et al. 1996). The most recent anal- low soils, those which have received little human dis-
ysis of the global C cycle by the Intergovernmental turbance (which presumably were close to input–output
Panel on Climate Change (IPCC) concluded that N de- balance prior to receiving enhanced N deposition), and
position could represent a major component of the those receiving experimental additions of N well above
missing C sink (Schimel et al. 1995). Further refine- ambient levels (e.g., Driscoll et al. 1987, Murdoch and
ments could come from more complete analyses of the Stoddard 1991, Kahl et al. 1993). In contrast, forests
fraction of anthropogenic N that is retained within ter- that have been subjected to intense or repeated biomass
restrial ecosystems, on regional to continental scales removals have very high capacities to retain N (Aber
(Galloway et al. 1995, Howarth et al. 1996). et al. 1995, Magill et al. 1997). The early stages of N
saturation have also been noted in response to elevated
Nitrogen saturation and ecosystem function N deposition in dry conifer forests surrounding the Los
Ultimately, there are declining returns in the re- Angeles Basin, California (Bytnerowicz and Fenn
sponse of plant production and carbon storage to ad- 1996), in the Front Range of the Colorado Rockies
ditions of N, and consequently the potential for eco- (Baron et al. 1994), and in forests in which symbiotic
systems to retain added N through increased production N-fixing organisms are major components (Van Mie-
and organic matter storage is limited. The term ‘‘ni- groet 1992). Nitrogen saturation is much further ad-
trogen saturation’’ (Ågren and Bosatta 1988, Aber et vanced over extensive areas of northern Europe, where
al. 1989, Aber 1992) has been applied to changes in N rates of anthropogenic N deposition are several-fold
cycling in forest ecosystems that occur as N limitations greater than the most extreme areas in North America
to biological functions are relieved by N additions. In (Berendse et al. 1993).
a fully N-saturated system (particularly one that is not Overall, the ability of a forest ecosystem to retain N
storing C for some other reason such as its stage of is linked to its productive potential, and the degree to
stand development, or increasing CO ), N losses to which previous disturbances have resulted in N re-2
streams, groundwater, and the atmosphere should ap- moval and current N limitations. Thus, the extent and
proach total N deposition, and any fertilization effects importance of N saturation are tightly linked to changes
or continued C storage should disappear. in land use, climate, atmospheric CO2 and O3, and other
Concerns regarding the effects of N deposition on environmental variables that are also subject to rapid
forest health and downstream ecosystems arose follow- change.
ing observation of significant increases in nitrate con-
Nitrogen deposition and changes in ecosystem
centrations in some lakes and streams (Grennfelt and
composition and biodiversity
Hultberg 1986, Henriksen and Brakke 1988, Stoddard
1994), and documented declines and mortality in co- The addition of limiting nutrients can dramatically
niferous evergreen forests in Europe (Schulze 1989). change which species are dominant in ecosystems and
These observations have led to several field experi- markedly decrease the overall biodiversity of ecosys-
ments that examined interactions between N deposition tems. For example, experimental additions of nitrogen
and forest ecosystem function (e.g., Van Miegrot et al. to grassland ecosystems in England have led to in-
1992, Kahl et al. 1993, Wright and van Breeman 1995, creased dominance by a few nitrogen-demanding grass
742 PETER M. VITOUSEK ET AL. Ecological ApplicationsVol. 7, No. 3
species, and to suppression of many other plant species
(Lawes and Gilbert 1880, Brenchley and Warington
1958, Thurston 1969, Silvertown 1980). The highest
rate of N loading caused the number of plant species
to decline more than five-fold. Similarly dramatic re-
ductions in plant diversity have been observed follow-
ing N loading in North American grasslands (Tilman
1987, 1996, Huenneke et al. 1990), European grass-
lands (Bobbink et al. 1988), and European heathlands
(Aerts and Berendse 1988).
Because of its high population density and inter-
weaving of intensive livestock operations and industry,
rates of N deposition in the Netherlands are the highest
in the world, averaging 4–9 g·m22·yr21. The conse-
quences of that enhanced deposition are well docu-
mented. Nitrogen deposition causes the conversion of
heathlands to species-poor grasslands and forest (Aerts
and Berendse 1988). Because heathlands occur on
sandy, nitrogen-poor soils, the effect of deposition is
to make heathlands more similar in composition to
plant communities that occupy more fertile soils. Thus,
biological diversity at the landscape level is reduced
by N deposition, just as species richness within com-
munities is reduced. FIG. 4. Export of total nitrogen (a) and nitrate (b) from
The loss of diversity caused by N deposition (or other river systems, as a function of human population density in
global changes) can affect other aspects of ecosystem the watershed. Reprinted from Howarth et al. (1996:Fig. 3a,
function. For example, recent experiments in the Mid- b) with permission of Kluwer Academic Publishers (where
Fig. 3b was modified from Peierls et al. [1991]). Note
western United States showed that productivity in spe- logarithmic scale.
cies-poor ecosystems that result from nitrogen addition
was much less stable when they experienced a major in the watersheds (Peierls et al. 1991, Cole et al. 1993)
drought (Tilman and Downing 1994). Similarly, the (Fig. 4).
most diverse plots experienced much less year-to-year No comparable historical data on the concentrations
variation in productivity in response to climatic vari- of total dissolved N in surface waters are available.
ation during non-drought years than did the most spe- Analyses of recent data suggest that N in streams and
cies-poor plots (Tilman 1996). rivers draining relatively undisturbed forests is largely
EFFECTS ON AQUATIC SYSTEMS organic N (Schindler et al. 1980, Hedin et al. 1995);
with increasing human disturbance, total N fluxes in
Historical changes in water chemistry rivers increase and a higher proportion is composed of
Given human-caused acceleration of N fixation and nitrate (Howarth et al 1996). Total N fluxes in rivers
other changes in N cycling, it is no surprise that N also are correlated with human population density, but
concentrations have increased over time in surface wa- the slope is much shallower for total N than NO3, il-
ters. In more-developed regions, nitrate concentrations lustrating the greater mobility of nitrate relative to oth-
have been more-or-less continuously measured in many er forms of N (Howarth et al 1996).
rivers and other drinking-water supplies for decades. Fluxes of total N in temperate-zone rivers surround-
Analysis of these data show that nitrate has more than ing the North Atlantic Ocean are highly correlated with
doubled in the Mississippi River since 1965 (Turner net anthropogenic inputs of N to their watersheds (Fig.
and Rabalais 1991, Justic et al. 1995), and that nitrate 5; r2 5 0.73, P 5 0.002; Howarth et al. 1996). Net
concentrations in major rivers in the northeastern U.S. anthropogenic N inputs are defined as the sum of inputs
have increased by 3- to 10-fold since the early 1900s as fertilizer, through N fixation by agricultural crops,
(N. Jaworski and R. W. Howarth, unpublished manu- as deposition of oxidized N from the atmosphere, and
script) Available evidence suggests similar trends for as the net import or export of N in food and feedstocks
many European rivers since the turn of the century (see also Jordan and Weller 1996). For this regional
(Paces 1982, Larsson et al. 1985), and Henriksen and analysis, N from sewage, N from animal feedlots, and
Brakke (1988) report a doubling of nitrate in 1000 Nor- NH4 deposition from the atmosphere were considered
wegian lakes in less than a decade. Moreover, nitrate to represent recycling of nitrogen within regions. For
fluxes and concentrations in the large rivers of the most of the regions surrounding the North Atlantic,
world are correlated with human population densities anthropogenic inputs of N are dominated by fertilizer,
August 1997 ALTERATION OF THE GLOBAL N CYCLE 743
FIG. 5. Export of total nitrogen from watersheds surrounding the North Atlantic Ocean, as a function of net anthropogenic
inputs of nitrogen to their watersheds. Net anthropogenic inputs are defined as (industrial N fertilizer 1 N fixation by legume
crops 1 atmospheric inputs of oxidized N 1 net imports of N in food and feedstock). Reprinted from Howarth et al. (1996:
Fig. 5a) with permission of Kluwer Academic Publishers.
but for the northeastern United States and the Saint cent reductions in SO2 emissions have reduced inputs
Lawrence River and Great Lakes basin, atmospheric of sulfuric acid to ecosystems, while emissions of the
deposition of oxidized nitrogen is the greatest input nitrogen oxides that are precursors of nitric acid have
(Fisher and Oppenheimer 1991, Howarth et al. 1996). gone unchecked. As a result of this shift, and the fact
Even though fertilizer inputs dominate in most regions, that many catchments in moderate- to high-deposition
overall N exports from the regions are better correlated areas appear to be becoming nitrogen saturated, nitric
with atmospheric deposition of oxidized N. acid is playing an increasing role in lake acidification.
Using relatively undisturbed areas as references, Ho- In addition, nitric acid is highly mobile in snowpacks
warth et al. (1996) estimated that riverine total N fluxes subjected to periodic melting, and in many areas it is
from most of the temperate regions surrounding the the predominant strong acid in the spring acid pulse
North Atlantic Ocean may have increased from pre- (Schaefer et al. 1990).
industrial times by 2- to 20-fold. For the North Sea Nitrogen contributes to acidity in two ways—nitric
region, the N increase may have been 6- to 20-fold.
acid does so directly, and ammonium deposited to ter-
Increased concentrations of nitrate have also been ob-
served in groundwater in many agricultural regions restrial and aquatic systems can be a further source of
(Moody 1990). The magnitude of this storage is dif- acidity, in that both biological uptake of ammonium
ficult to determine, outside of a few well-characterized and nitrification produce hydrogen ions (Schindler et
aquifers. Overall, the annual increment of N added to al. 1985, Schuurkes and Mosello 1988, Johnson et al.
groundwater probably represents a small fraction of the 1991). Moreover, where human alteration of the N cy-
increased nitrate transported in surface waters (Ho- cle induces nitrate loss, the nitrate is a mobile anion
warth et al. 1996), but the long residence time of that can move through soils to streams and ground-
groundwater in many aquifers means that decreases in water, pulling cations with it and thereby depleting the
groundwater quality are likely to continue as long as soil of calcium and other nutrients (Likens et al. 1970,
human effects on the N cycle are substantial. 1996). As calcium is depleted the leaching of toxic
Nitrate in drinking water represents a human health inorganic aluminum is increased. In N-saturated areas
concern—when levels are high, microorganisms in the of Europe, a substantial fraction of atmospheric nitrate
stomach may convert nitrate to nitrite. Nitrite absorbed moves through terrestrial ecosystems without ever be-
into the bloodstream converts hemoglobin to methe- ing taken up by organisms (Durka et al. 1994). The
moglobin, which is ineffective in oxygen transport in effects of acidity, and of the mobilization of aluminum
the blood. Acute and chronic elevated methemoglobin that it causes, on aquatic systems have been reviewed
can kill infants, in a condition known as methemoglo- by Irving (1990) and others. In areas without much
binemia (Lee 1970). Although the disease is rare in the acid-neutralizing capacity, they are clear and profound.
U.S., the potential for methemoglobinemia exists The crucial point is that recent increases in the fixation
whenever nitrate levels exceed 10 mg N/L—the U.S. and emission of N, and the increasing extent of N-sa-
Public Health Service standard.
turated ecosystems, mean that controlling emissions of
Nitrogen and acidification compounds that produce sulfuric acid will be insuffi-
The interaction between nitrogen deposition and cient to decrease acid rain or its effects on streams and
freshwater acidification is complex. In many areas, re- lakes (Posch et al. 1995). The importance of N in acid-
744 PETER M. VITOUSEK ET AL. Ecological ApplicationsVol. 7, No. 3
ifying ecosystems is clearly recognized in Europe,
where intergovernmental efforts are underway to re-
duce N emissions and deposition on a regional basis
(DoE 1994). Critical loads (threshold levels) for nitro-
gen are considered to be an important part of managing
acid precipitation there (Nilsson and Grennfelt 1988),
and wetlands and riparian areas are being restored in
an attempt to prevent excess nitrogen from entering
freshwater and coastal zones (Leonardson 1994). An
approach based on critical loads may not be appropriate
conceptually for some of the consequences of N de-
position—it is not clear there are thresholds for all of
these effects—but critical loads may nonetheless rep-
resent a useful tool for managing N deposition.
Acidification itself can also disrupt the nitrogen cy-
cle in freshwater ecosystems. In experimental lakes in FIG. 6. Primary production (PP) by phytoplankton (14C
Ontario, nitrification of ammonium ceased at pH values uptake) as a function of the estimated rate of input of dis-
below 5.6 (Rudd et al. 1988), while higher nitrate in- solved inorganic nitrogen (DIN) per unit area in a variety of
marine ecosystems. Natural systems are represented by solid
puts stimulated aquatic denitrification (Rudd et al. circles; open circles are for large (13 m3, 5 m deep), well-
1990). Nitrogen fixation in Little Rock Lake ceased at mixed mesocosm tanks at the Marine Ecosystems Research
pH , 5, but no effect on nitrification was observed Laboratory during a multi-year fertilization experiment. Re-
(Schindler et al. 1991). printed from Nixon et al. (1996:Fig. 5) with permission of
In freshwater ecosystems with sufficient phosphorus, Kluwer Academic Publishers.
additions of inorganic nitrogen can cause eutrophica-
tion; this can occur either independently or coupled to seas (NRC 1993). There is good evidence for increasing
acidification (Schindler et al. 1985). Decreased diver- anoxia since the 1950s or 1960s for the Baltic Sea
sity of both animal and plant species generally accom- (Larsson et al. 1985), the Black Sea (Lein and Ivanov
panies both eutrophication and acidification (Schindler 1992), and Chesapeake Bay (Officer et al. 1984). Hyp-
1990, 1994). oxic events have increased in Long Island Sound (Par-
ker and O’Reilly 1991), the North Sea (Rosenberg
Fertilization and eutrophication in estuaries and 1985), and the Kattegat (Baden et al. 1990); low-
coastal seas oxygen problems have resulted in significant losses of
The eutrophication of estuaries and coastal seas is fish and shellfish resources (Baden et al. 1990, Hansson
one of the best-documented and best-understood con- and Rudstam 1990, NRC 1993).
sequences of human-altered N cycling (Howarth 1988, Eutrophication is also associated with a loss of di-
NRC 1993, Justic et al. 1995, Nixon 1995, Nixon et versity, both in the benthic community and among
al. 1996); it represents perhaps the greatest threat to planktonic organisms (Howarth 1991). Among phyto-
the integrity of coastal ecosystems (NRC 1993, 1994). plankton, this can be manifested by dominance of nui-
In most temperate-zone estuaries and coastal seas, net sance algae. An increased incidence of nuisance algal
primary production and eutrophication are controlled blooms has been observed in many estuaries and coast-
by nitrogen inputs (Fig. 6; Boynton et al. 1982, D’Elia al seas, and although the reasons are not completely
et al. 1986, Howarth et al. 1995, Nixon et al. 1996). known, compelling evidence suggests that increased
Some areas are controlled by P rather than N, partic- nutrient supplies are responsible at least in part (Smay-
ularly tropical lagoons where adsorption onto carbon- da 1989, NRC 1993). Toxic blooms of dinoflagellates
ate sands provides a major sink for phosphate, and in (Anderson 1989, Burkholder et al. 1992) and of brown-
some temperate estuaries and seas that receive extreme- tide organisms (Cosper et al. 1987) during the 1980s
ly high loading of N (Howarth et al. 1995). Most often, were responsible for extensive mortality of fish and
however, eutrophication is caused by anthropogenic N shellfish in many estuaries. Eutrophication can also
loading—in sharp contrast to the majority of lakes in lead to a loss of diversity in subtidal beds of macro-
the temperate zone, where phosphorus is the element algae, in seagrass beds, and in corals (NRC 1993).
most limiting net primary production and controlling
eutrophication (Schindler 1977). MAJOR UNCERTAINTIES
Eutrophication has substantial effects on ecosystem This analysis has focused on describing the scientific
function and composition in estuaries. It can cause an- consensus on global change in the N cycle—in other
oxia (no oxygen) or hypoxia (low oxygen) in stratified words, what is known, and how we know it. There are
waters, and both anoxia and hypoxia appear to be be- also major uncertainties in our knowledge of the N
coming more prevalent in many estuaries and coastal cycle and how it relates to other aspects of global
August 1997 ALTERATION OF THE GLOBAL N CYCLE 745
change; we highlight a few of the most fundamental fact that all of Earth is more or less affected by human
ones here. It is always possible, and often valuable, to activity. Nevertheless, studies in remote southern hemi-
improve estimates of a regional or global process; here, sphere temperate regions (Galloway et al. 1982, Hedin
however, we focus on important processes that are et al. 1995) illustrate that valuable information on areas
known so poorly as to make it difficult to detect an- that have been minimally altered by humans remains
thropogenic global change, or to predict its conse- to be gathered.
quences.
Alteration of denitrification
Marine N fixation
At the scale of large river basins, the majority of
Credible estimates of the rate of N fixation in marine nitrogen inputs to a region probably are denitrified (Ho-
ecosystems range over more than a factor of 10 (Gal- warth et al. 1996). Our understanding of the locus of
loway et al. 1995); as a consequence, the state of sci- this denitrification is inadequate, although it is clear
entific understanding of both current and background that riparian areas and wetlands make important con-
N fixation in the ocean is insufficient to evaluate the tributions. Human activity has influenced the quantity
extent or global significance of any human-caused and distribution of denitrification—enhancing it by
global change in marine N fixation. There is some ev- adding nitrate to ecosystems, by building dams, and by
idence that human alteration of the N cycle could alter cultivating rice; decreasing it by draining wetlands and
biological processes in the open ocean (Knap et al. altering riparian areas—but these changes remain poor-
1986, Cornell et al. 1995, Michaels et al. 1996), but it ly characterized.
is difficult to evaluate this possibility given our lack
of understanding of the unmodified N cycle in the open FUTURE PROSPECTS AND MANAGEMENT OPTIONS
oceans. Globally, most of the anthropogenic enhancement of
Changing resource limitation N fixation is closely tied to human activities related to
food production. Intensive agricultural systems require
One consequence of human alteration of the global large quantities of fixed N; humanity requires intensive
N cycle is that many ecosystems in which biological agriculture to support our growing (and urbanizing)
processes once were limited by N supply now receive population; and our population is likely to double (or
large inputs of nitrogen, causing limitation by other more) by the end of the next century. Moreover, N
resources to become more important. The dominant fertilizer is a relatively inexpensive commodity, and a
species in these systems may have evolved with nitro- decision to apply fertilizer is often the least expensive
gen limitation; the ways they grow and function, and and most effective option to increase agricultural yield.
their symbiotic partners, could be highly tuned to it. The production and application of N has grown ex-
How is the performance of organisms and ecosystems ponentially, and the highest rates of application are
affected by shifts in resource limitation to conditions found in some developing countries with the highest
with which they have no evolutionary background, and rates of population growth (Matthews 1994). Galloway
to which they are not adapted? et al. (1994) suggest that by 2020 the global production
of nitrogen fertilizer will increase to 134 Tg N/yr, from
Nitrogen retention capacity
a current level of about 80 Tg N/yr. Clearly, curtailing
There is substantial variation in the capacity of forest anthropogenic fixation of N will be a very difficult
ecosystems and wetlands to retain added N. A number challenge.
of interacting factors that correlate with a system’s ca- Nevertheless, there are prospects for slowing growth
pacity to retain N (prior to becoming N saturated) have in the amount of N fixed for agriculture, and for re-
been identified, including the C:N ratio of soil organic ducing the mobility (and hence consequences) of the
matter, soil texture and degree of chemical weathering, N that is applied. While the use of fixed N in agriculture
fire history, rate of biomass accumulation, and past cannot be substituted, there are reasons to believe that
human land use. Connections between ecosystems the efficiency of N fertilizer can be increased substan-
within landscapes can also affect losses of N to aquatic tially. A relatively large fraction of applied N (often
systems and the atmosphere. However, we lack a fun- half or more) is typically lost from agricultural systems
damental understanding of how and why the processes as N2, trace gases, and nitrate; from a local viewpoint
that retain N vary among systems, and how they have this is an expensive waste, while from a broader per-
changed and will change with time. spective it is a significant driver of global change. A
number of management practices that can increase the
Background N deposition and loss efficiency of fertilizer N have been recognized. To the
While information on current rates of N deposition extent that these can be developed, improved, and im-
and loss in developed regions is improving steadily, plemented widely, some human fixation of N can be
our understanding of these fluxes prior to extensive foregone. For example, Matson et al. (1996) evaluated
human effects is still patchy. In part, this reflects the N trace-gas flux in two commercial sugar cane plan-
746 PETER M. VITOUSEK ET AL. Ecological ApplicationsVol. 7, No. 3
tations in Hawaii. One applied N in several split ap- geochemistry and primary production altered by nitrogen
plications, with increasing quantities of N timed to the saturation. Water Air and Soil Pollution 85:1665–1670.
Aber, J. D., K. J. Nadelhoffer, P. Steudler, and J. M. Melillo.
requirements of the growing crop. Fertilizer was dis- 1989. Nitrogen saturation in northern forest ecosystems.
solved in irrigation water, which was delivered under BioScience 39:378–386.
the soil surface. The other plantation used fewer, larger Aerts, R., and F. Berendse. 1988. The effect of increased
applications of fertilizer N broadcast onto the soil sur- nutrient availability on vegetation dynamics in wet heath-
face. The more knowledge-intensive system used 2/3 lands. Vegetatio 76:63–69.Ågren, G. I., and E. Bosatta. 1988. Nitrogen saturation of
as much N per crop as the more fertilizer-intensive terrestrial ecosystems. Environmental Pollution 54:185–
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forms of N as well) were 10-fold less than from the Albritton, D. L., R. G. Derwent, I. S. A. Isaksen, M. Lal, and
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ACKNOWLEDGMENTS Boxman, A. W., D. van Dam, H. F. G. van Dyck, R. F. Hog-
We thank the Pew Charitable Trusts for financial support ervorst and C. J. Koopmans. 1995. Ecosystem responses
provided through a Pew Scholars Fellowship to David Til- to reduced nitrogen and sulphur inputs into two coniferous
man; we thank Steve Carpenter, Judy Meyer, and Lou Pitelka forest stands in the Netherlands. Forest Ecology and Man-
for thoughtful comments on the manuscript; and we thank agement 71:7–30.
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