Human Alteration of the Global Nitrogen Cycle: Causes and ...

Human Alteration of theGlobal Nitrogen Cycle:

Causes and Consequences

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SUMMARY

Human activities are greatly increasing the amount of nitrogen cycling between the living world and the soil, water, andatmosphere. In fact, humans have already doubled the rate of nitrogen entering the land-based nitrogen cycle, and thatrate is continuing to climb. This human-driven global change is having serious impacts on ecosystems around the worldbecause nitrogen is essential to living organisms and its availability plays a crucial role in the organization and functioningof the world�s ecosystems. In many ecosystems on land and sea, the supply of nitrogen is a key factor controlling thenature and diversity of plant life, the population dynamics of both grazing animals and their predators, and vital ecologi-cal processes such as plant productivity and the cycling of carbon and soil minerals. This is true not only in wild orunmanaged systems but in most croplands and forestry plantations as well. Excessive nitrogen additions can polluteecosystems and alter both their ecological functioning and the living communities they support.

Most of the human activities responsible for the increase in global nitrogen are local in scale, from the production and useof nitrogen fertilizers to the burning of fossil fuels in automobiles, power generation plants, and industries. However,human activities have not only increased the supply but enhanced the global movement of various forms of nitrogenthrough air and water. Because of this increased mobility, excess nitrogen from human activities has serious and long-term environmental consequences for large regions of the Earth.

The impacts of human domination of the nitrogen cycle that we have identified with certainty include:

• Increased global concentrations of nitrous oxide (N2O), a potent greenhouse gas, in the atmosphere aswell as increased regional concentrations of other oxides of nitrogen (including nitric oxide, NO) thatdrive the formation of photochemical smog;

• Losses of soil nutrients such as calcium and potassium that are essential for long-term soil fertility;• Substantial acidification of soils and of the waters of streams and lakes in several regions;• Greatly increased transport of nitrogen by rivers into estuaries and coastal waters where it is a major

pollutant.

We are also confident that human alterations of the nitrogen cycle have:

• Accelerated losses of biological diversity, especially among plants adapted to low-nitrogen soils, andsubsequently, the animals and microbes that depend on these plants;

• Caused changes in the plant and animal life and ecological processes of estuarine and nearshoreecosystems, and contributed to long-term declines in coastal marine fisheries.

National and international policies should attempt to reduce these impacts through the development and widespreaddissemination of more efficient fossil fuel combustion technologies and farm management practices that reduce theburgeoning demand for and release of nitrogenous fertilizers.

Human Alteration of theGlobal Nitrogen Cycle:

Causes and Consequences

Issues in Ecology Number 1 Spring 1997

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INTRODUCTION

This report presents an overview of the currentscientific understanding of human-driven changes to theglobal nitrogen cycle and their consequences. It alsoaddresses policy and management options that could helpmoderate these changes in the nitrogen cycle and theirimpacts.

THE NITROGEN CYCLE

Nitrogen is an essential component of proteins,genetic material, chlorophyll, and other key organic mol-ecules. All organisms require nitrogen in order to live. Itranks fourth behind oxygen, carbon, and hydrogen asthe most common chemical element in living tissues. Untilhuman activities began to alter the natural cycle (Figure1), however, nitrogen was only scantily available to muchof the biological world. As a result, nitrogen served as

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Human Alteration of the Global Nitrogen Cycle:Causes and Consequences

byPeter M. Vitousek, Chair, John Aber, Robert W. Howarth,Gene E. Likens, Pamela A. Matson, David W. Schindler,

William H. Schlesinger, and G. David Tilman

one of the major limiting factors that controlled the dy-namics, biodiversity, and functioning of many ecosystems.

The Earth�s atmosphere is 78 percent nitrogengas, but most plants and animals cannot use nitrogengas directly from the air as they do carbon dioxide andoxygen. Instead, plants � and all organisms from thegrazing animals to the predators to the decomposers thatultimately secure their nourishment from the organicmaterials synthesized by plants � must wait for nitro-gen to be �fixed,� that is, pulled from the air and bondedto hydrogen or oxygen to form inorganic compounds,mainly ammonium (NH4) and nitrate (NO3), that theycan use.

The amount of gaseous nitrogen being fixed atany given time by natural processes represents only asmall addition to the pool of previously fixed nitrogenthat cycles among the living and nonliving componentsof the Earth�s ecosystems. Most of that nitrogen, too,is unavailable, locked up in soil organic matter � par-

Figure 1-Simplified diagram of the nitrogen cycle. Adapted from Environmental Science, Third Edition by JonathonTurk and Amos Turk, 81984 by Saunders College Publishing, reproduced by permission of the publisher.

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a million metric tons of nitrogen. Worldwide, lightning,for instance, fixes less than 10 Tg of nitrogen per year� maybe even less than 5 Tg. Microbes are the majornatural suppliers of new biologically available nitrogen.Before the widespread planting of legume crops, terres-trial organisms probably fixed between 90 and 140 Tgof nitrogen per year. A reasonable upper bound for therate of natural nitrogen fixation on land is thus about140 Tg of N per year.

HUMAN-DRIVEN NITROGEN FIXATION

During the past century, human activities clearlyhave accelerated the rate of nitrogen fixation on land,effectively doubling the annual transfer of nitrogen fromthe vast but unavailable atmospheric pool to the biologi-cally available forms. The major sources of this enhancedsupply include industrial processes that produce nitro-gen fertilizers, the combustion of fossil fuels, and thecultivation of soybeans, peas, and other crops that hostsymbiotic nitrogen-fixing bacteria. Furthermore, humanactivity is also speeding up the release of nitrogen fromlong-term storage in soils and organic matter.

tially rotted plant and animal remains � that must bedecomposed by soil microbes. These microbes releasenitrogen as ammonium or nitrate, allowing it to be re-cycled through the food web. The two major naturalsources of new nitrogen entering this cycle are nitrogen-fixing organisms and lightning.

Nitrogen-fixing organisms include a relativelysmall number of algae and bacteria. Many of them livefree in the soil, but the most important ones are bacteriathat form close symbiotic relationships with higher plants.Symbiotic nitrogen-fixing bacteria such as the Rhizobia,for instance, live and work in nodules on the roots ofpeas, beans, alfalfa and other legumes. These bacteriamanufacture an enzyme that enables them to convertgaseous nitrogen directly into plant-usable forms.

Lightning may also indirectly transform atmo-spheric nitrogen into nitrates, which rain onto soil.

Quantifying the rate of natural nitrogen fixationprior to human alterations of the cycle is difficult butnecessary for evaluating the impacts of human-drivenchanges to the global cycling of nitrogen. The standardunit of measurement for analyzing the global nitrogencycle is the teragram (abbreviated Tg), which is equal to

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Figure 2-Nitrogen is the major factor limiting many terrestrial ecosystems, including most of those in thetemperate zone, such as this oak savannah. The number and identities of the plant and animal species thatlive in such terrestrial ecosystems, and the functioning of the ecosystem, depends on the rate of nitrogensupply to the ecosystem.

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Nitrogen FertilizerIndustrial fixation of nitrogen for use as fertilizer

currently totals approximately 80 Tg per year and repre-sents by far the largest human contribution of new nitro-gen to the global cycle (Figure 3). That figure does notinclude manures and other organic nitrogen fertilizers,which represent a transfer of already-fixed nitrogen fromone place to another rather than new fixation.

The process of manufacturing fertilizer by indus-trial nitrogen fixation was first developed in Germanyduring World War I, and fertilizer production has grownexponentially since the 1940s. In recent years, the in-creasing pace of production and use has been truly phe-nomenal. The amount of industrially fixed nitrogen ap-plied to crops during the decade from 1980 to 1990more than equaled all industrial fertilizer applied previ-ously in human history.

Until the late 1970s, most industrially producedfertilizer was applied in developed countries. Use in theseregions has now stabilized while fertilizer applications indeveloping countries have risen dramatically. The mo-mentum of human population growth and increasing ur-banization ensures that industrial fertilizer production willcontinue at high and likely accelerating rates for decadesin order to meet the escalating demand for food.

Nitrogen-Fixing CropsNearly one third of the Earth�s land surface is

devoted to agricultural and pastoral uses, and humanshave replaced large areas of diverse natural vegetationwith monocultures of soybeans, peas, alfalfa, and otherleguminous crops and forages. Because these plants sup-port symbiotic nitrogen-fixers, they derive much of their

nitrogen directly from the atmosphere and greatly in-crease the rate of nitrogen fixation previously occurringon those lands. Substantial levels of nitrogen fixationalso occur during cultivation of some non-legumes, nota-bly rice. All of this represents new, human-generatedstocks of biologically available nitrogen. The quantity ofnitrogen fixed by crops is more difficult to analyze thanindustrial nitrogen production. Estimates range from 32to 53 Tg per year. As an average, 40 Tg will be usedhere.

Fossil Fuel BurningThe burning of fossil fuels such as coal and oil

releases previously fixed nitrogen from long-term stor-age in geological formations back to the atmosphere inthe form of nitrogen-based trace gases such as nitricoxide. High-temperature combustion also fixes a smallamount of atmospheric nitrogen directly. Altogether, theoperations of automobiles, factories, power plants, andother combustion processes emit more than 20 Tg peryear of fixed nitrogen to the atmosphere. All of it istreated here as newly fixed nitrogen because it has beenlocked up for millions of years and would remain lockedup indefinitely if not released by human action.

Mobilization of Stored NitrogenBesides enhancing fixation and releasing nitro-

gen from geological reservoirs, human activities also lib-erate nitrogen from long-term biological storage poolssuch as soil organic matter and tree trunks, contributingfurther to the proliferation of biologically available nitro-gen. These activities include the burning of forests, woodfuels, and grasslands, which emits more than 40 Tg per

Figure 3-The pace of many hu-man-caused global changes hasincreased starkly in modern his-tory, but none so rapidly as in-dustrial production of nitrogenfertilizer, which has grown ex-ponentially since the 1940s.The chart shows the year whichchanges in human populationgrowth, carbon dioxide release,deforestation, and fertilizer pro-duction had reached 25%,50%, and 75% of the extentseen in the late 1980s. Revisedfrom Kates et al. (1990).

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Sources of Human-Caused Alteration to the Global Nitrogen Cycle


year of nitrogen; the draining of wetlands, which setsthe stage for oxidation of soil organic matter that couldmobilize 10 Tg per year or more of nitrogen; and landclearing for crops, which could mobilize 20 Tg per yearfrom soils.

There are substantial scientific uncertainties aboutboth the quantity and the fate of nitrogen mobilized bysuch activities. Taken together, however, they could con-tribute significantly to changes in the global nitrogencycle.

Human Versus Natural Nitrogen FixationOverall, fertilizer production, legume crops, and

fossil fuel burning deposit approximately 140 Tg of newnitrogen into land-based ecosystems each year, a figurethat equals the upper estimates for nitrogen fixed natu-rally by organisms in these ecosystems. Other humanactivities liberate and make available half again that muchnitrogen. From this evidence, it is fair to conclude thathuman activities have at least doubled the transfer ofnitrogen from the atmosphere into the land-based bio-logical nitrogen cycle.

This extra nitrogen is spread unevenly across theEarth�s surface: Some areas such as northern Europe arebeing altered profoundly while others such as remote re-gions in the Southern Hemisphere receive little direct in-put of human-generated nitrogen. Yet no region remainsunaffected. The increase in fixed nitrogen circulatingaround the globe and falling to the ground as wet or drydeposition is readily detectable, even in cores drilled fromthe glacial ice of Greenland.

IMPACTS ON THE ATMOSPHERE

One major consequence of human-driven alter-ations in the nitrogen cycle has been regional and globalchange in the chemistry of the atmosphere (Figure 4) �specifically, increased emissions of nitrogen-based tracegases such as nitrous oxide, nitric oxide, and ammonia(NH3). Although such releases have received less atten-tion than increased emissions of carbon dioxide and vari-ous sulfur compounds, the trace nitrogen gases causeenvironmental effects both while airborne and after theyare deposited on the ground. For instance, nitrous oxideis long-lived in the atmosphere and contributes to thehuman-driven enhancement of the greenhouse effect thatlikely warms the Earth�s climate. Nitric oxide is an im-portant precursor of acid rain and photochemical smog.

Some of the human activities discussed aboveaffect the atmosphere directly. For instance, essentially

all of the more than 20 Tg per year of fixed nitrogenreleased in automobile exhausts and in other emissionsfrom fossil fuel burning is emitted to the atmosphere asnitric oxide. Other activities indirectly enhance emissionsto the atmosphere. Intensive fertilization of agriculturalsoils can increase the rates at which nitrogen in the formof ammonia is volatilized and lost to the air. It can alsospeed the microbial breakdown of ammonium and nitratesin the soil, enhancing the release of nitrous oxide. Evenin wild or unmanaged lands downwind of agricultural orindustrial areas, rain or windborne deposition of human-generated nitrogen can spur increased emissions of ni-trogen gases from the soils.

Nitrous OxideNitrous oxide is a very effective heat-trapping

gas in the atmosphere, in part because it absorbs outgo-ing radiant heat from the Earth in infrared wavelengthsthat are not captured by the other major greenhousegases, water vapor and carbon dioxide. By absorbingand reradiating this heat back toward the Earth, nitrousoxide contributes a few percent to overall greenhousewarming.

Although nitrous oxide is unreactive and long-lived in the lower atmosphere, when it rises into the strato-sphere it can trigger reactions that deplete and thin thestratospheric ozone layer that shields the Earth fromdamaging ultraviolet radiation.

The concentration of nitrous oxide in the atmo-sphere is currently increasing at the rate of two- to three-tenths of a percent per year. While that rise is clearlydocumented, the sources of the increase remain unre-solved. Both fossil fuel burning and the direct impactsof agricultural fertilization have been considered and re-jected as the major source. Rather, there is a developingconsensus that a wide array of human-driven sourcescontribute systematically to enrich the terrestrial nitro-gen cycle. These �dispersed sources� include fertilizers,nitrogen-enriched groundwater, nitrogen-saturated for-ests, forest burning, land clearing, and even the manu-facture of nylon, nitric acid, and other industrial prod-ucts.

The net effect is increased global concentrationsof a potent greenhouse gas that also contributes to thethinning of the stratospheric ozone layer.

Nitric Oxide and AmmoniaUnlike nitrous oxide, which is unreactive in the

lower atmosphere, both nitric oxide and ammonia arehighly reactive and therefore much shorter lived. Thus

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EFFECTS ON THE CARBON CYCLE

Increased emissions of airborne nitrogen have ledto enhanced deposition of nitrogen on land and in theoceans. Thanks to the fertilizer effects of nitrogen instimulating plant growth, this deposition may be actingto influence the atmosphere indirectly by altering the glo-bal carbon cycle.

Over much of the Earth�s surface, the lushnessof plant growth and the accumulation of standing stocksof plant material historically have been limited by scantynitrogen supplies, particularly in temperate and borealregions. Human activity has substantially increased thedeposition of nitrogen over much of this area, which raisesimportant questions: How much extra plant growth hasbeen caused by human-generated nitrogen additions? Asa result, how much extra carbon has been stored in ter-restrial ecosystems rather than contributing to the risingconcentrations of carbon dioxide in the atmosphere?

Answers to these questions could help explainthe imbalance in the carbon cycle that has come to beknown as the �missing sink.� The known emissions ofcarbon dioxide from human activities such as fossil fuelburning and deforestation exceed by more than 1,000Tg the amount of carbon dioxide known to be accumu-lating in the atmosphere each year. Could increasedgrowth rates in terrestrial vegetation be the �sink� thataccounts for the fate of much of that missing carbon?

Experiments in Europe and America indicate thata large portion of the extra nitrogen retained by forest,wetland, and tundra ecosystems stimulates carbon up-take and storage. On the other hand, this nitrogen can

changes in their atmospheric concentrations can be de-tected only at local or regional scales.

Nitric oxide plays several critical roles in atmo-spheric chemistry, including catalyzing the formation ofphotochemical (or brown) smog. In the presence of sun-light, nitric oxide and oxygen react with hydrocarbonsemitted by automobile exhausts to form ozone, the mostdangerous component of smog. Ground-level ozone hasserious detrimental effects on human health as well asthe health and productivity of crops and forests.

Nitric oxide, along with other oxides of nitrogenand sulfur, can be transformed in the atmosphere intonitric acid and sulfuric acid, which are the major compo-nents of acid rain.

Although a number of sources contribute to ni-tric oxide emissions, combustion is the dominant one.Fossil fuel burning emits more than 20 Tg per year ofnitric oxide. Human burning of forests and other plantmaterial may add about 10 Tg, and global emissions ofnitric oxide from soils, a substantial fraction of which arehuman-caused, total 5 to 20 Tg per year. Overall, 80percent or more of nitric oxide emissions worldwide aregenerated by human activities, and in many regions theresult is increased smog and acid rain.

In contrast to nitric oxide, ammonia acts as theprimary acid-neutralizing agent in the atmosphere, hav-ing an opposite influence on the acidity of aerosols,cloudwater, and rainfall. Nearly 70 percent of globalammonia emissions are human-caused. Ammonia vola-tilized from fertilized fields contributes an estimated 10Tg per year; ammonia released from domestic animalwastes about 32 Tg; and forest burning some 5 Tg.

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Figure 4-Human activities are responsible for alarge proportion of the global emissions of ni-trogen-containing trace gases, including 40%of the nitrous oxide, 80% or more of nitric ox-ide, and 70% of ammonia releases. The result isincreasing atmospheric concentrations of thegreenhouse gas nitrous oxide, of the nitrogenprecursors of smog, and of biologically availablenitrogen that falls from the atmosphere to fertil-ize ecosystems. Ammonia data are fromSchlesinger and Hartley (1992), nitric oxide fromDelmas et al. (in press), and nitrous oxide fromPrather et al. (1995).


Ammonia(NH )3

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Human-Caused Global Nitrogen Emissions

tems. These impacts first be-came apparent in Europe almosttwo decades ago when scientistsobserved significant increases innitrate concentrations in somelakes and streams and also ex-tensive yellowing and loss ofneedles in spruce and other co-nifer forests subjected to heavynitrogen deposition. These ob-servations led to several field ex-periments in the U.S. and Eu-rope that have revealed a com-plex cascade of effects set inmotion by excess nitrogen in for-est soils.

As ammonium builds upin the soil, it is increasingly con-verted to nitrate by bacterialaction, a process that releaseshydrogen ions and helps acidifythe soil. The buildup of nitrateenhances emissions of nitrousoxides from the soil and also en-courages leaching of highly wa-ter-soluble nitrate into streamsor groundwater. As these nega-tively charged nitrates seep

away, they carry with them positively charged alkalineminerals such as calcium, magnesium, and potassium.Thus human modifications to the nitrogen cycle decreasesoil fertility by greatly accelerating the loss of calciumand other nutrients that are vital for plant growth. Ascalcium is depleted and the soil acidified, aluminum ionsare mobilized, eventually reaching toxic concentrationsthat can damage tree roots or kill fish if the aluminumwashes into streams. Trees growing in soils replete withnitrogen but starved of calcium, magnesium, and potas-sium can develop nutrient imbalances in their roots andleaves. This may reduce their photosynthetic rate andefficiency, stunt their growth, and even increase treedeaths.

Nitrogen saturation is much further advancedover extensive areas of northern Europe than in NorthAmerica because human-generated nitrogen depositionis several times greater there than in even the most ex-tremely affected areas of North America. In the nitro-gen-saturated ecosystems of Europe, a substantial frac-tion of atmospheric nitrate deposits move from the landinto streams without ever being taken up by organisms

also stimulate microbial decom-position and thus releases of car-bon from soil organic matter.On balance, however, the car-bon uptake through new plantgrowth appears to exceed thecarbon losses, especially in for-ests.

A number of groupshave attempted to calculate theamount of carbon that could bestored in terrestrial vegetationthanks to plant growth spurredby added nitrogen. The result-ing estimates range from 100to 1,300 Tg per year. The num-ber has tended to increase inmore recent analyses as themagnitude of human-drivenchanges in the nitrogen cyclehas become clearer. The mostrecent analysis of the globalcarbon cycle by the Intergovern-mental Panel on Climate Changeconcluded that nitrogen depo-sition could represent a majorcomponent of the missing car-bon sink.

More precise estimates will become possible whenwe have a more complete understanding of the fractionof human-generated nitrogen that actually is retainedwithin various land-based ecosystems.

NITROGEN SATURATION ANDECOSYSTEM FUNCTIONING

There are limits to how much plant growth canbe increased by nitrogen fertilization. At some point,when the natural nitrogen deficiencies in an ecosystemare fully relieved, plant growth becomes limited by spar-sity of other resources such as phosphorus, calcium, orwater. When the vegetation can no longer respond tofurther additions of nitrogen, the ecosystem reaches astate described as �nitrogen saturation.� In theory, whenan ecosystem is fully nitrogen-saturated and its soils,plants, and microbes cannot use or retain any more, allnew nitrogen deposits will be dispersed to streams,groundwater, and the atmosphere.

Nitrogen saturation has a number of damagingconsequences for the health and functioning of ecosys-

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Figure 5-Wild plants living in natural ecosystems,such as this lupine, a nitrogen-fixing plant, domi-nated the nitrogen cycle for millions of years. Hu-man production of nitrogen fertilizer, burning of fossilfuels, and intensive cultivation of legume crops nowadds as much nitrogen to terrestrial ecosystems asdo all natural processes combined.


this constraint. New supplies of nitrogen showered uponthese ecosystems can cause a dramatic shift in the domi-nant species and also a marked reduction in overall spe-cies diversity as the few plant species adapted to takefull advantage of high nitrogen out compete their neigh-bors. In England, for example, nitrogen fertilizers ap-plied to experimental grasslands have led to increaseddominance by a few nitrogen-responsive grasses and lossof many other plant species. At the highest fertilizationrate, the number of plant species declined more than five-fold. In North America, similarly dramatic reductions inbiodiversity have been created by fertilization of grass-lands in Minnesota and California (Figures 7, 8, and 9).In formerly species-rich heathlands across Western Eu-rope, human-driven nitrogen deposition has been blamedfor great losses of biodiversity in recent decades.

In the Netherlands, high human population den-sity, intensive livestock operations, and industries havecombined to generate the highest rates of nitrogen depo-sition in the world. One well-documented consequencehas been the conversion of species-rich heathlands to spe-cies-poor grasslands and forest. Not only the speciesrichness of the heath but also the biological diversity ofthe landscape has been reduced because the modifiedplant communities now resemble the composition of com-munities occupying more fertile soils. The unique speciesassemblage adapted to sandy, nitrogen-poor soils is be-ing lost from the region.

or playing a role in the biological cycle.In contrast, in the northeastern U.S., increased

leaching of nitrates from the soil and large shifts in thenutrient ratios in tree leaves generally have been observedonly in certain types of forests. These include high-el-evation sites that receive large nitrogen deposits and siteswith shallow soils containing few alkaline minerals tobuffer acidification. Elsewhere in the U.S., the early stagesof nitrogen saturation have been seen in response to el-evated nitrogen deposition in the forests surrounding theLos Angeles Basin and in the Front Range of the Colo-rado Rockies.

Some forests have a very high capacity to retainadded nitrogen, particularly regrowing forests that havebeen subjected to intense or repeated harvesting, an ac-tivity that usually causes severe nitrogen losses. Over-all, the ability of a forest to retain nitrogen depends onits potential for further growth and the extent of its cur-rent nitrogen stocks. Thus, the impacts of nitrogen depo-sition are tightly linked to other rapidly changing hu-man-driven variables such as shifts in land use, climate,and atmospheric carbon dioxide and ozone levels.

EFFECTS ON BIODIVERSITY AND THE SPECIES MIX

Limited supplies of biologically available nitrogenare a fact of life in most natural ecosystems, and manynative plant species are adapted to function best under

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Figure 6-Deposition of nitrogen from the atmosphere is believed to be responsible for the yellow-ing and loss of needles from conifers and for cases of forest dieback, such as that shown here.

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Losses of biodiversity driven by nitrogen deposi-tion can in turn affect other ecological processes. Re-cent experiments in Minnesota grasslands showed thatin ecosystems made species-poor by fertilization, plantproductivity was much less stable in the face of a majordrought. Even in non-drought years, the normal vagar-ies of climate produced much more year-to-year varia-tion in the productivity of species-poor grassland plotsthan in more diverse plots.

EFFECTS ON AQUATICECOSYSTEMS

Historical Changes in WaterChemistry

Not surprisingly, ni-trogen concentrations in sur-face waters have increased ashuman activities have acceler-ated the rate of fixed nitrogenbeing put into circulation. Arecent study of the North At-lantic Ocean Basin by scien-tists from a dozen nations es-timates that movements of to-tal dissolved nitrogen intomost of the temperate-zonerivers in the basin may haveincreased by two- to 20-foldsince preindustrial times (Fig-ure 10). For rivers in the NorthSea region, the nitrogen in-crease may have been six- to20-fold. The nitrogen in-creases in these rivers arehighly correlated with human-generated inputs of nitrogen to their watersheds, andthese inputs are dominated by fertilizers and atmosphericdeposition.

For decades, nitrate concentrations in many riv-ers and drinking water supplies have been closely moni-tored in developed regions of the world, and analysis ofthese data confirms a historic rise in nitrogen levels inthe surface waters. In 1,000 lakes in Norway, for ex-ample, nitrate levels doubled in less than a decade. Inthe Mississippi River, nitrates have more than doubledsince 1965. In major rivers of the northeastern U.S.,nitrate concentrations have risen three- to ten-fold sincethe early 1900s, and the evidence suggests a similartrend in many European rivers.

Again not surprisingly, nitrate concentrations inthe world�s large rivers rise along with the density ofhuman population in the watersheds. Amounts of totaldissolved nitrogen in rivers are also correlated with hu-man population density, but total nitrogen does not in-crease as rapidly as the nitrate fraction. Evidence indi-cates that with increasing human disturbance, a higherproportion of the nitrogen in surface waters is composedof nitrate.

Increased concentrationsof nitrate have also been ob-served in groundwater inmany agricultural regions, al-though the magnitude of thetrend is difficult to determinein all but a few well-charac-terized aquifers. Overall, theadditions to groundwaterprobably represent only asmall fraction of the increasednitrate transported in surfacewaters. However, groundwa-ter has a long residence timein many aquifers, meaningthat groundwater quality islikely to continue to decline aslong as human activities arehaving substantial impacts onthe nitrogen cycle.

High levels of nitrates indrinking water raise signifi-cant human health concerns,especially for infants. Mi-crobes in an infant�s stomachmay convert high levels of ni-trate to nitrite. When nitrite

is absorbed into the bloodstream, it converts oxygen-carrying hemoglobin into an ineffective form called meth-emoglobin. Elevated methemoglobin levels � an anemiccondition known as methemoglobinemia � can causebrain damage or death. The condition is rare in the U.S.,but the potential exists whenever nitrate levels exceedU.S. Public Health Service standards (10 milligrams perliter).

Nitrogen and Acidification of LakesNitric acid is playing an increasing role in the

acidification of lakes and streams for two major reasons.One is that most efforts to control acid deposition �which includes acid rain, snow, fog, mist, and dry depos-

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Figure 7-Different rates of nitrogen addition lead tomarked changes in the plant and insect species com-positions and speicies diversity of these plots of grass-land vegetation in Minnesota. Each plot is 4m x 4m(about 13 ft x 13 ft), and has received experimentaladdition of nitrogen (ammonium nitrate) since 1982.

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its � have focused on cutting emissions of sulfur diox-ide to limit the formation of sulfuric acid in the atmo-sphere. In many areas, these efforts have succeeded inreducing inputs of sulfuric acid to soils and water whileemissions of nitrogen oxides, the precursors of nitric acid,have gone largely unchecked. The second reason is thatmany watersheds in areas of moderate to high nitrogendeposition appear to be approaching nitrogen saturation,and the increasingly acidified soils have little capacity tobuffer acid rain before it enters streams.

An additional factor in many areas is that nitricacid predominates among the pollutants that accumu-late in the winter snowpack. Much of this nitric acid isflushed out with the first batch of spring meltwater, of-ten washing a sudden, concentrated �acid pulse� intovulnerable lakes.

Adding inorganic nitrogen to freshwater ecosys-tems that are also rich in phosphorus can eutrophy aswell as acidify the waters. Both eutrophication and acidi-fication generally lead to decreased diversity of both plantand animal species. Fish populations, in particular, havebeen reduced or eliminated in many acidified lakes acrossScandinavia, Canada, and northeastern United States.

Because the extent of nitrogen-saturated ecosys-tems continues to grow, along with human-caused nitro-gen deposition, controls on sulfur dioxide emissions aloneclearly will not be sufficient to decrease acid rain or pre-vent its detrimental effects on streams and lakes. Euro-pean governments already have recognized the impor-tance of nitrogen in acidifying soils and waters, and in-tergovernmental efforts are underway there to reduceemissions and deposition of nitrogen on a regional basis.

Eutrophication in Estuaries and Coastal WatersOne of the best documented and best understood

consequences of human alterations of the nitrogen cycleis the eutrophication of estuaries and coastal seas (Fig-ure 11 and 12). It is arguably the most serious humanthreat to the integrity of coastal ecosystems.

In sharp contrast to the majority of temperate-zone lakes, where phosphorus is the nutrient that mostlimits primary productivity by algae and other aquaticplants and controls eutrophication, these processes arecontrolled by nitrogen inputs in most temperate-zone es-tuaries and coastal waters. This is largely because thenatural flow of nitrogen into these waters and the rate ofnitrogen fixation by planktonic organisms are relativelylow while microbes in the sea floor sediments activelyrelease nitrogen back to the atmosphere.

When high nitrogen loading causes eutrophica-tion in stratified waters � where a sharp temperaturegradient prevents mixing of warm surface waters withcolder bottom waters � the result can be anoxia (nooxygen) or hypoxia (low oxygen) in bottom waters. Bothconditions appear to be becoming more prevalent in manyestuaries and coastal seas. There is good evidence thatsince the 1950s or 1960s, anoxia has increased in theBaltic Sea, the Black Sea, and Chesapeake Bay. Periods

Figure 8-Native grasslands in Minnesota often contain 20to 30 or more plant species per square meter, as does thisplot. This plot is a �control� plot that received no nitrogen,and that retained its original plant diversity.

Figure 9-Nitrogen addition to this plot, located near that shownin Figure 8, led to the loss of almost all native prairie speciesand to dominance by the weedy European quackgrass. In1982 this plot looked much like the one shown in Figure 8.

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year. There is some evidence that human alteration ofthe nitrogen cycle could alter biological processes in theopen ocean, but there is no adequate frame of referenceagainst which to evaluate any potential human-drivenchange in marine nitrogen fixation.

Changes in Limiting ResourcesOne consequence of human-driven changes in the

global nitrogen cycle is a shift in the resources that limitbiological processes in many areas. Large amounts ofnitrogen are now deposited on many ecosystems thatwere once nitrogen deficient. The dominant species inthese systems may have evolved with nitrogen limita-tion, and the ways they grow and function and formsymbiotic partnerships may reflect adaptations to thislimit. With this limit removed, species must operate un-der novel constraints such as now-inadequate phospho-rus or water supplies. How are the performance of or-ganisms and the operation of larger ecological processesaffected by changes in their chemical environment forwhich they have no evolutionary background and to whichthey are not adapted?

Capacity to Retain NitrogenForests and wetlands vary substantially in their

capacity to retain added nitrogen. Interacting factorsthat are known to affect this capacity include soil tex-ture, degree of chemical weathering of soil, fire history,rate at which plant material accumulates, and past hu-man land use. However, we still lack a fundamental un-derstanding of how and why nitrogen-retention processesvary among ecosystems � much less how they havechanged and will change with time.

of hypoxia have increased in Long Island Sound, the NorthSea, and the Kattegat, resulting in significant losses offish and shellfish.

Eutrophication is also linked to losses of diver-sity, both in the sea floor community � includingseaweeds, seagrasses, and corals � and among plank-tonic organisms. In eutrophied waters, for example, �nui-sance algae� may come to dominate the phytoplanktoncommunity. Increases in troublesome or toxic algal bloomshave been observed in many estuaries and coastal seasworldwide in recent decades. During the 1980s, toxicblooms of dinoflagellates and brown-tide organismscaused extensive die-offs of fish and shellfish in manyestuaries. Although the causes are not completely un-derstood, there is compelling evidence that nutrient en-richment of coastal waters is at least partly to blame forsuch blooms.

MAJOR UNCERTAINTIES

Although this report has focused on what isknown about human-driven changes to the global nitro-gen cycle, major uncertainties remain. Some of thesehave been noted in earlier sections. This section, how-ever, focuses on important processes that remain so poorlyunderstood that it is difficult to distinguish human-causedimpacts or to predict their consequences.

Marine Nitrogen FixationLittle is known about the unmodified nitrogen

cycle in the open ocean. Credible estimates of nitrogenfixation by organisms in the sea vary more than ten-fold,ranging from less than 30 to more than 300 Tg per

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Figure 10-Movements of nitro-gen into most of the temperate-zone rivers that empty into theNorth Atlantic Ocean have in-creased by two to 20-fold sincepreindustrial times. Nitrogen in-creases in these rivers are highlycorrelated with increasing human-generated nitrogen inputs intothe watersheds, particularly fer-tilizer use and rising atmosphericdeposition of nitrogen. Modifiedfrom Howarth et al. (1996).


Alteration of DenitrificationIn large river basins, the majority of nitrogen that

arrives is probably broken down by denitrifying bacteriaand released to the atmosphere as nitrogen gas or ni-trous oxide. Exactly where most of this activity takesplace is poorly understood, although we know that stream-side areas and wetlands are important. Human activitiessuch as increased nitrate deposition, dam building, andrice cultivation have probably enhanced denitrification,while draining of wetlands and alteration of riparian eco-systems has probably decreased it. But the net effect ofhuman influence remains uncertain.

Natural Nitrogen CyclingInformation on the rate of nitrogen depo-

sition and loss in various regions prior to extensivehuman alterations of the nitrogen cycle remainspatchy. In part, this reflects the fact that all of theEarth already is affected to some degree by hu-man activity. Nevertheless, studies in remote re-gions of the Southern Hemisphere illustrate thatthere is still valuable information to be gathered onareas that have been minimally altered by humans.

FUTURE PROSPECTS ANDMANAGEMENT OPTIONS

Fertilizer UseThe greatest human-driven increases in glo-

bal nitrogen supplies are linked to activities intendedto boost food production. Modern intensive agri-

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culture requires large quantities of nitrogen fertil-izer; humanity, in turn, requires intensive agricul-ture to support a growing population that is pro-jected to double by the end of the next century.Consequently, the production and application ofnitrogen fertilizer has grown exponentially, and thehighest rates of application are now found in somedeveloping countries with the highest rates of popu-lation growth. One study predicts that by theyear 2020, global production of nitrogen fertil-izer will increase from a current level of about 80Tg to 134 Tg per year.Curtailing this growth in nitrogen fertilizer pro-

duction will be a difficult challenge. Nevertheless,there are ways to slow the growth of fertilizer useand also to reduce the mobility � and hence theregional and global impacts � of the nitrogenthat is applied to fields.One way to reduce the amount of fertilizer used

is to increase its efficiency. Often at least half of thefertilizer applied to fields is lost to the air or water. Thisleakage represents an expensive waste to the farmer aswell as a significant driver of environmental change. Anumber of management practices have been identifiedthat can reduce the amounts of fertilizer used and cutlosses of nitrogen to the air and water without sacrific-ing yields or profits (and in some cases, increasing them).For instance, one commercial sugar cane plantation inHawaii was able to cut nitrogen fertilizer use by one thirdand reduce losses of nitrous oxide and nitric oxide ten-

Figure 11-The bottom-dwelling plants of a marine ecosystemthat received natural rates of nitrogen addition. Note the highdiversity of these plants and their spacing.

Figure 12-The bottom-dwelling plants of a marine ecosystem thatreceived high rates of nitrogen input. Note that there are fewplant species, and that the leaves of these are covered with athick layer of algae.

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ing world. One study predicts that production of nitro-gen oxides from fossil fuels will more than double in thenext 25 years, from about 20 Tg per year to 46 Tg.Reducing these emissions will require improvements inthe efficiency of fuel combustion as well as in the inter-ception of airborne byproducts of combustion. As withimprovements in fertilizer efficiency, it will be particularlyimportant to transfer efficient combustion technologiesto developing countries as their economies and indus-tries grow.

CONCLUSIONS

Human activities during the past century havedoubled the natural annual rate at which fixed nitrogenenters the land-based nitrogen cycle, and the pace is likelyto accelerate. Serious environmental consequences arealready apparent. In the atmosphere, concentrations ofthe greenhouse gas nitrous oxide and of the nitrogen-precursors of smog and acid rain are increasing. Soils inmany regions are being acidified and stripped of nutri-ents essential for continued fertility. The waters of streamsand lakes in these regions are also being acidified, andexcess nitrogen is being transported by rivers into estu-aries and coastal waters. It is quite likely that this un-precedented nitrogen loading has already contributed to

fold by dissolving the fertilizer in irrigation water, deliv-ering it below the soil surface, and timing multiple appli-cations to meet the needs of the growing crop. Thisknowledge-intensive system also proved more profitablethan broadcasting fewer, larger applications of fertilizeronto the soil surface. The widespread implementation ofsuch practices, particularly in developing regions, shouldbe a high priority for agronomists as well as ecologistssince improved practices provide an opportunity to re-duce the costs of food production while slowing the rateof global change.

There are also ways to prevent the nitrogen thatleaches from fertilized farmland from reaching streams,estuaries and coastal waters where it contributes toeutrophication. In many regions, agricultural lands havebeen expanded by channelizing streams, clearing ripar-ian forests, and draining wetlands. Yet these areas serveas important natural nitrogen traps. Restoration of wet-lands and riparian areas and even construction of artifi-cial wetlands have been shown to be effective in prevent-ing excess nitrogen from entering waters.

Fossil Fuel BurningThe second major source of human-fixed nitro-

gen is fossil fuel burning. It, too, will increase markedlyas we enter the next century, particularly in the develop-

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Figure 13-Human activities, such as fertilizer production, growing legume crops, and burning of fossil fuels, are nowof equal or greater magnitude than natural processes in the nitrogen cycle. Human domination of the nitrogen cycleimpacts the functioning of many terrestrial and aquatic ecosystems, including seemingly pristine habitats such as thisalpine ecosystem.


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Nixon, S. W., J. W. Ammerman, L. P. Atkinson, V. M.Berounsky, G. Billen, W. C. Boicourt, W. R. Boynton, T.M. Church, D. M. Ditoro, R. Elmgren, J. H. Garber, A.E. Giblin, R. A. Jahnke, N. P. J. Owens, M. E. Q. Pilson,and S. P. Seitzinger. The fate of nitrogen and phosphorusat the land-sea margin of the North Atlantic Ocean. Bio-geochemistry 35: 141-180.

NRC. 1994. Priorities for Coastal Ecosystem Science.National Research Council. Washington, D.C.

Prinn, R., D. Cunnold, R. Rasmussen, P. Simmonds, F.Alyca, A. Crawford, P. Fraser, and R. Rosen. 1990. At-mospheric emissions and trends of nitrous oxide deducedfrom 10 years of ALE-GAGE data. Journal of Geophysi-cal Research 95:18,369-18,385.

Schindler, D. W. and S. E. Bayley. 1993. The biosphereas an increasing sink for atmospheric carbon:estimatesfrom increasing nitrogen deposition. Global Biogeochemi-cal Cycles 7:717-734.

Schlesinger, W. H. 1991. Biogeochemistry: An Analysisof Global Change. Academic Press, San Diego.

Smil, V. 1991. Population growth and nitrogen: an ex-ploration of a critical existential link. Population andDevelopment Review 17:569-601.

Tamm, C. O. 1991. Nitrogen in Terrestrial Ecosystems.Springer-Verlag, Berlin. 115 pp.

Tilman, D. 1987. Secondary succession and the patternof plant dominance along experimental nitrogen gradi-ents. Ecological Monographs 57(3):189-214.

Vitousek, P. M. and R. W. Howarth. 1991. Nitrogenlimitation on land and in the sea: How can it occur? Bio-geochemistry 13:87-115.

About the Panel of ScientistsThis report presents the consensus reached by a

panel of eight scientists chosen to include a broad arrayof expertise in this area. This report underwent peerreview and was approved by the Board of Editors of Is-sues in Ecology. The affiliations of the members of thepanel of scientists are:

Dr. Peter M. Vitousek, Panel Chair, Department of Bio-logical Sciences, Stanford University, Stanford, CA 94305

long-term declines in coastal fisheries and acceleratedlosses of plant and animal diversity in both aquatic andland-based ecosystems. It is urgent that national andinternational policies address the nitrogen issue, slow thepace of this global change, and moderate its impacts.

FOR FURTHER INFORMATION

This report summarizes the findings of our panel.Our full report, which is being published in the journalEcological Applications (Volume 7, August 1997), dis-cusses and cites more than 140 references to the pri-mary scientific literature on this subject. From that listwe have chosen those below as illustrative of the scien-tific publications and summaries upon which our reportis based.

Aber, J.D. 1992. Nitrogen cycling and nitrogen satura-tion in temperate forest ecosystems. Trends in Ecologyand Evolution 7:220-223.

Berendse, F., R. Aerts, and R. Bobbink. 1993. Atmo-spheric nitrogen deposition and its impact on terrestrialecosystems. Pp. 104-121 in C.C. Vos and P. Opdam(eds), Landscape Ecology of a Stressed Environment.Chapman and Hall, England.

Cole, J. J., B. L. Peierls, N. F. Caraco, and M. L. Pace.1993. Nitrogen loadings of rivers as a human-driven pro-cess. Pages 141-157 in M. J. McDonnell and S. T. A.Picket (eds.), Humans as Components of Ecosystems:The Ecology of Subtle Human Effects and Populated Ar-eas. Springer-Verlag, NY.

DOE (Department of Environment, UK). 1994. Impactsof Nitrogen Deposition in Terrestrial Ecosystems. Techni-cal Policy Branch, Air Quality Div., London.

Galloway, J. N., W. H. Schlesinger, H. Levy II, A. Michaels,and J. L. Schnoor. 1995. Nitrogen fixation: atmosphericenhancement-environmental response. Global Bio-geochemical Cycles 9:235-252.

Howarth, R. W., G. Billen, D. Swaney, A. Townsend, N.Jaworski, K. Lajtha, J. A. Downing, R. Elmgren, N.Caraco, T. Jordan, F. Berendse, J. Freney, V. Kudeyarov,P. Murdoch, and Zhu Zhao-liang. 1996. Regional nitro-gen budgets and riverine N & P fluxes for the drainagesto the North Atlantic Ocean: Natural and human influ-ences. Biogeochemistry 35: 75-139.

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ogy, Evolution and Behavior, University of Minnesota,St. Paul, MN 55108-6097. E-mail: [email protected]

Board membersDr. Stephen Carpenter, Center for Limnology, University

of Wisconsin, Madison, WI 53706Dr. Deborah Jensen, The Nature Conservancy, 1815

North Lynn Street, Arlington, VA 22209Dr. Simon Levin, Department of Ecology & Evolutionary

Biology, Princeton University, Princeton, NJ08544-1003

Dr. Jane Lubchenco, Department of Zoology, OregonState University, Corvallis, OR 97331-2914

Dr. Judy L. Meyer, Institute of Ecology, The University ofGeorgia, Athens, GA 30602-2202

Dr. Gordon Orians, Department of Zoology, Universityof Washington, Seattle, WA 98195

Dr. Lou Pitelka, Appalachian Environmental Laboratory,Gunter Hall, Frostburg, MD 21532

Dr. William Schlesinger, Departments of Botany andGeology, Duke University, Durham, NC 27708-0340

Additional CopiesTo receive additional copies of this report, please

contact:

Public Affairs OfficeEcological Society of America

2010 Massachusetts Avenue, NWSuite 400

Washington, DC [email protected]

(202) 833-8773

This version of the report is also available electronicallyat http://www.sdsc.edu/~ESA/.

Also available for a small fee are reprints of ourfull report, published in the journal Ecological Applica-tions (Volume 7, August 1997) with detailed citations tothe original scientific literature. Contact the EcologicalSociety of America at the above listed address for moreinformation.

Special thanks to the U.S. Environmental Protec-tion Agency for supporting printing and distribution ofthis document.

Dr. John Aber, Complex Systems Research Center, Insti-tute for the Study of Earth, Oceans and Space, Univer-sity of New Hampshire, Durham, NH 03824-3525

Dr. Robert W. Howarth, Section of Ecology and System-atics, Corson Hall, Cornell University, Ithaca, NY 14853

Dr. Gene E. Likens, Institute of Ecosystem Studies, CaryArboretum, Millbrook, NY 12545

Dr. Pamela A. Matson, Soil Science, University of Cali-fornia, Berkeley, Berkeley, CA 94720

Dr. David W. Schindler, Department of Biological Sciences,University of Alberta, Edmonton, Alberta, T6G 2E9,CANADA

Dr. William H. Schlesinger, Departments of Botany andGeology, Duke University, Durham, NC 27708-0340

Dr. David Tilman, Department of Ecology, Evolution andBehavior, University of Minnesota, St. Paul, MN 55108-6097

About the Science WriterYvonne Baskin, a science writer, edited the re-

port of the panel of scientists to allow it to more effec-tively communicate its findings with non-scientists.

About Issues in EcologyIssues in Ecology is designed to report, in lan-

guage understandable by non-scientists, the consensusof a panel of scientific experts on issues relevant to theenvironment. Issues in Ecology is supported by a PewScholars in Conservation Biology grant to David Tilmanand by the Ecological Society of America. All reportsundergo peer review and must be approved by the edito-rial board before publication.

AcknowledgementsThis series was inspired by Dr. Ron Pulliam, who

first proposed the idea, and Dr. Judy Meyer who chairedan Ecological Society of America committee that devel-oped the concepts and convinced ESA to pursue it. Wegratefully acknowledge their contributions. We also thankFaith Kearns for her assistance with design and produc-tion of this issue.

Editorial Board of Issues in EcologyDr. David Tilman, Editor-in-Chief, Department of Ecol-

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About Issues in Ecology

Issues in Ecology is designed to report, in language understandable by non-scientists, theconsensus of a panel of scientific experts on issues relevant to the environment. Issues inEcology is supported by the Pew Scholars in Conservation Biology program and by the Eco-logical Society of America. It is published at irregular intervals, as reports are completed. Allreports undergo peer review and must be approved by the Editorial Board before publication.

Issues in Ecology is an official publication of the Ecological Society of America, the nation�sleading professional society of ecologists. Founded in 1915, ESA seeks to promote theresponsible application of ecological principles to the solution of environmental problems.For more information, contact the Ecological Society of America, 2010 Massachusetts Av-enue, NW, Suite 400, Washington, DC, 20036. ISSN 1092-8987

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