environews focus - robert b. laughlinlarge.stanford.edu/courses/2015/ph240/chen-lh1/docs/...states,...

A 556 VOLUME 112 | NUMBER 10 | July 2004 • Environmental Health Perspectives

Environews Focus

Environmental Health Perspectives • VOLUME 112 | NUMBER 10 | July 2004 A 557

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Focus | Global Nitrogen

Cycling out of Control

GLOBALNITROGEN

L ike the Earth’s water, nitrogen compounds cycle through the air,aquatic systems, and soil. But unlike water, these compounds arebeing injected into the environment in ever increasing quantities.

In doing so, we are altering the global nitrogen cycle, causing possiblegrave impacts on biodiversity, global warming, water quality, humanhealth, and even the rate of population growth in developing nations.

In a world surrounded by nitrogen, you would think there’s alwaysbeen plenty to go around and that perhaps a little more wouldn’t matter.But having enough of the right kind of nitrogen—reactive nitrogen thathas been “fixed,” or converted from the nonreactive N2 form—deter-mines such fundamentals of life as the extent of plant growth, which inturn determines to a large extent the dynamics of the world’s food sup-ply. During the twentieth century, mankind has produced increasinglymore reactive nitrogen, intentionally as fertilizer and unintentionally as aby-product of combusting fossil fuels.

Although carbon dioxide may get more press, “the nitrogen cycle hasbeen altered more than any other basic element cycle,” says John Aber,vice president for research and public service at the University of NewHampshire. And now, he says, humans are adding more reactive nitrogento the global nitrogen cycle than all other sources combined. Yet, reactivenitrogen is hardly all bad. The use of nitrogen fertilizer is critical to feed-ing the world’s hungry, say researchers including University of Virginia

environmental sciences professor JamesGalloway. The question, then, is how do wemanage nitrogen responsibly?

A Natural History of NitrogenEverything that lives needs nitrogen. Butmost atoms of nitrogen—which represents78% of the atmosphere—are bound tightlyin pairs as N2. Most organisms can’t breakthe powerful triple bond of the N2 mole-cule’s two atoms. For plants to grow andanimals to thrive, they need the element ina reactive fixed form that is bonded to car-bon, hydrogen, or oxygen, most often asorganic nitrogen compounds (such asamino acids), ammonium (NH4), or nitrate(NO3). Animals get their reactive nitrogenfrom eating plants and other animals some-where along the food chain. And plants getreactive nitrogen from the soil or water.

Lightning accounts for some naturallyoccurring reactive nitrogen—worldwideeach year, lightning fixes an estimated

3–10 teragrams (Tg), the usual measure-ment unit for discussing the global nitro-gen cycle. The energy that lightning gen-erates converts oxygen and nitrogen tonitric oxide (NO), which oxidizes to nitro-gen dioxide (NO2), then to nitric acid(HNO3). Within days the HNO3 is car-ried to the ground in rain, snow, hail, orother atmospheric deposition. This sourceof reactive nitrogen is important to areasin which nitrogen-fixing plants are scarce.

Most naturally occurring reactive nitro-gen comes from nitrogen fixation by bacte-ria, including cyanobacteria and specializedbacteria such as those in the genusRhizobium, which most often live symbiot-ically in plants such as peas, beans, andalfalfa. According to a literature reviewpublished in the April 2003 issue ofBioScience by Galloway and colleagues,experts believe natural, nonagriculturalorganisms fix 100–300 Tg of nitrogen peryear on the land surfaces of the Earth,

although most estimates tend toward thelower end.

Farmers eventually learned to increasethe levels of reactive nitrogen in their soilusing plants that have nitrogen-fixing bac-terial symbionts, but their resources werelimited: at the beginning of the twentiethcentury they could rotate with nitrogen-fixing crops such as legumes, or add natu-rally occurring fertilizers such as manure,guano, and nitrate mineral deposits minedin Chile. At this point, according to theBioScience review, humans were producingabout 15 Tg of reactive nitrogen per year.

Around this time, however, Germanscientists Fritz Haber and Carl Bosch devel-oped a way to convert nonreactive atmos-pheric nitrogen to ammonia, the reactivecompound that forms the base of nitrogenfertilizer. Currently, the Haber-Boschprocess is used to produce about 100 Tg ofreactive nitrogen per year worldwide, mostof which is used to produce nitrogen fertil-izer. Food grown with this fertilizer feedssome 2 billion people, estimates VaclavSmil, a professor of geography at theUniversity of Manitoba, writing in the July1997 issue of Scientific American.

The past 15 years have seen a hugeexplosion in the amount of reactive nitro-gen that humans have produced and inject-ed into the environment, according to areport on relationships between the globalnitrogen cycle and human health in volume1, issue 5 (2003) of Frontiers in Ecology andthe Environment by Alan Townsend, anassistant professor of ecology and evolu-tionary biology at the University ofColorado, and colleagues. Human produc-tion of reactive nitrogen is currently esti-mated to be about 170 Tg per year, writeGalloway and colleagues in the BioSciencereview, and the global use of nitrogen fertil-izers is increasing by about 15 Tg per year.The ratio of anthropogenic to natural reac-tive nitrogen creation is likely to increasewith population increases, Galloway says.More mouths to feed will require bothmore reactive nitrogen fertilizers in theground and the clearing of unspoiled,nitrogen-fixing lands to make farmland.

Human Sources of ReactiveNitrogenWhere does all this human-generated reac-tive nitrogen come from? The largest con-tributor is nitrogen fertilizer. As of 2000,about 100 Tg of reactive nitrogen werereleased each year from nitrogen fertilizerspread on farmlands around the world,according to the BioScience review. Asmodern farming methods have beenincreasingly adopted, so has the rate atwhich nitrogen is being fixed, with much of


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Food for a hungry world. Food grown with nitrogen fertilizers feeds an estimated 2 billion peo-ple worldwide. Areas including Asia are becoming increasingly dependent on such fertilizers, tothe detriment of the environment.

the increase coming in developing coun-tries, according to Townsend and colleaguesin Frontiers in Ecology and Environment. Intheir BioScience review, Galloway and col-leagues write that widespread cultivation ofnitrogen-fixing crops such as legumes hasadded another approximately 40 Tg of reac-tive nitrogen.

Burning of biomass—the use of woodfor fuel and the clearing of forests and grass-lands for agriculture—converts another 40Tg or so. Draining wetlands allows organicmaterial in the soil to oxidize, and clearingland of vegetation for crops can free reactivenitrogen from soils. These sources con-tribute about 10 and 20 Tg, respectively,according to an article in the Spring 1997Issues in Ecology by a team led by PeterVitousek, a professor of population andresource studies at Stanford University.

Fossil fuel combustion also contributesto the reactive nitrogen load. “It’s not justagriculture that’s changing the nitrogencycle,” says Michael Mallin, a research pro-fessor at the University of North Carolina atWilmington’s Center for Marine Science.“Urbanization is doing it in a big way. Citiesare full of cars. Cars release nitrogen oxides[NOx; the collective term for NO andNO2]. It goes up into the air and comesdown as somebody else’s problem.” By fix-ing atmospheric nitrogen and releasing reac-tive nitrogen that otherwise would besequestered indefinitely in fuels, fossil fuelcombustion contributes about 20 Tg ofreactive nitrogen globally each year.

Very few parts of the Earth now lack theirown regional sources of reactive nitrogen pol-lution, says David Tilman, a professor of

ecology at the University of Minnesota.“Agricultural expansion has really taken overthe whole world,” he says. “The rates of fer-tilization per hectare—the nitrogen addedper hectare—are not that different. Not justamong the seven or eight most industrializednations, but even among nations that are notindustrial giants, the agricultural side hasreally pursued nitrogen fertilization.”Galloway adds that nitrogen pollution is dis-tributed globally not just by wind and waterbut also by ship and truck: “Internationalcommerce is a major way of shipping reactivenitrogen around the world,” he says.

As a result, Galloway says, there are sig-nificant sources of polluting reactive nitro-gen in just about any corner of the Earth,with the unfortunate exception of much ofAfrica, which although spared much directnitrogen pollution, is also deprived of thesorely needed fertilizer. Currently Asia,Europe, and North America account foralmost 90% of human-generated reactivenitrogen, Galloway says. European coun-tries such as the Netherlands (wherelong-term nitrogen fertilizer use and manyconcentrated animal farms have createdperhaps the world’s most nitrogen-saturatedarea) and Germany have long shown theeffects of nitrogen pollution. In theNetherlands, for example, extreme reactivenitrogen levels have changed the Dutchcountryside’s characteristic heathlands tograsslands. But over the next 50 years,Galloway says, the developing world’s grow-ing dependence on nitrogen fertilizers, ris-ing population densities, and adoption ofgasoline-powered vehicles are all likely toresult in increases in nitrogen-related envi-ronmental and human health impacts.

A Vicious Cycle?“The nitrogen cycle has changed on a glob-al scale to a remarkable extent, but the rateat which that plays out locally is hugelyvariable,” says Townsend. “There are majorhot spots at all of the industrialized nationsof the world. We’re seeing incredibleincreases [in reactive nitrogen use/produc-tion and resulting pollution] in the UnitedStates, much of Europe, and much of Asiaand China now. There are areas there, forexample, that are seeing deposition from


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Source: Lambert KF, Driscoll C. 2003. Nitrogen Pollution: From the Sources to the Sea. Hanover, NH: Hubbard Brook Research Foundation; 4.

The beauty of storms. Lightning is responsible for fixing a portion of the Earth’s naturally occur-ing reactive nitrogen, which is important for the soil in areas with few nitrogen-fixing plants.

the atmosphere that is tentimes or more what it wasprior to human activity.”

Some of this reactivenitrogen is, of course, putto good use, Townsendsays. Nitrogen fertilizerscan take credit for reduc-tions in starvation and mal-nutrition in many parts ofthe world, especially inAsia in the last decade. Infact, Smil writes in theMarch 2002 issue of theSwedish journal Ambio that“for at least a third ofhumanity in the world’smost populous countriesthe use of [nitrogen] fertil-izers makes the differencebetween malnutrition andadequate diet.”

But as nitrogen levelscontinue to rise, Townsendsays, the net health effectsbecome increasingly nega-tive. Furthermore, saysGalloway, reactive nitrogencan not only impact manydifferent ecosystems, but asingle atom also can make mischief repeat-edly, unlike most better recognized pollu-tants. “If you put a molecule of NOx in theatmosphere from fossil fuel combustion ora molecule of ammonium on an agricultur-al field as a fertilizer,” he explains, “you havea whole series, or cascade, of effects thatgoes from acid rain to particle formation inthe atmosphere, decreasing visibility andcausing impacts on human health, acidrain, soil and stream acidification, coastaleutrophication, decreasing biodiversity,human health issues in groundwater, andnitrous oxide [N2O] emissions to theatmosphere, which impact the greenhouseeffect and stratospheric ozone.”

Nitrogen in the AirThe effects of reactive nitrogen on ozoneare profound, wreaking havoc at every ele-vation. “In areas like the northeasternUnited States, because we have more auto-mobiles than agriculture, our major contri-bution to global nitrogen cycling is oxidizedforms of nitrogen,” Aber says. NOx, whichcan form from the application of nitrogenfertilizers, burning of biomass, and com-bustion of fossil fuels, is an important con-tributor to the formation of smog andground-level ozone. “That’s [the North-east’s] most important form of air pollu-tion,” Aber says.

High concentrations of NOx, which arecommon in urban areas with their high car

populations, can produce low-lying ozone,which in turn can cause or worsen asthma,cough, reactive airways disease, respiratorytract inflammation, and chronic respiratorydisease. High levels of NOx can also worsenviral infections such as the common cold.In addition to ground-level sources, wheredenitrification (the conversion of reactivenitrogen to N2) in soil also produces someN2O, aircraft inject NOx directly into theatmosphere.

At mid-altitudes, N2O acts as a green-house gas, with each molecule absorbingabout 200 times as much outgoing radia-tion as carbon dioxide. And although at lowaltitudes reactive nitrogen increases ozone,at very high altitudes it actually destroysozone. In the stratosphere, ultraviolet lightbreaks N2O apart, producing NO, whichin turn acts as a catalyst to break downozone. Destroying ozone in the strato-sphere, of course, allows more ultravioletlight to reach the Earth’s surface, resultingin more skin cancers—an article in the 30March 1998 International Journal ofClimatology by Rajaram P. Kane, a seniorscientist at the Brazilian National Institutefor Space Research, says that reductions inozone suggest a 10–20% increase in ultravi-olet-B radiation, which would “explain a20–40% rise in skin cancer in the humanpopulation since the 1970s.”

The effects of N2O can persist fordecades, with a residence time of 120 years

in the atmosphere, says Robert Howarth, aprofessor of ecology and environmentalbiology at Cornell University. “It plays a bigrole in catalyzing the destruction of ozonein the stratosphere,” he explains. “It’s agreenhouse gas, and it’s a pretty potentgreenhouse gas—it’s the longest-livedgreenhouse gas in the atmosphere.” Once inthe atmosphere, other nitrogen gases suchas NOx and ammonia can also generate par-ticulates that are small enough to penetratedeep into the lungs, contributing to cardio-vascular diseases, respiratory diseases, asth-ma, reduced lung function, and overallmortality.

In spite of the severity of these effects,Howarth says, there is little understandingamong the public of nitrogen’s role in pub-lic health, global warming, or much else.“Everyone on the street is well aware ofground-level ozone and that it is a serioushealth issue,” he says. “The average personon the street does not know that ozone pol-lution is caused by nitrogen pollution. Ifyou did not have the nitrogen pollution,you would not have the ozone pollution.”Other indirect health effects of nitrogenpollution include promotion of the condi-tions favorable to cholera and the breedingconditions for the types of mosquitoes thatcarry West Nile virus, malaria, andencephalitis.

Other experts point to a lack of recog-nition—in U.S. policy-making circles, at


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A good thing gone awry? Nitrogen fertilizers make the difference between an adequate diet and malnutrition formuch of the world population, but an excess of reactive nitrogen compounds in the air, water, and soil wreaks havocon fragile ecosystems.


least—of the role of reactive nitrogen inproducing acid rain. Not all NOx staysaloft, says Aber. “In contact with moisturein the atmosphere, it turns into nitric acid,which is the nitrogen component of acidrain,” he says. In industrialized areas of theUnited States, nitric acid has become anincreasingly significant component of acidraid, says Gene Likens, director of theInstitute of Ecosystem Studies in Mill-brook, New York. “Our long-term studiesat Hubbard Brook Experimental Forest—the longest continuous measurement ofprecipitation and stream-water chemistry inthe world—clearly indicate that there is amajor change under way,” he says. In 1963,when the studies began, he says, sulfuricacid contributed about 70% of total acidityof rain, and nitric acid was about 15%.Currently sulfuric acid is about 50%, andnitric acid is about 40%. “We project that ifthe current trends continue, nitric acid willbecome the dominant acid in eastern NorthAmerica by about 2012,” Likens says. “Andyet we’ve focused all of our regulations pri-marily on reducing sulfur.”

Nitrogen in the WaterIf any aspect of nitrogen pollution has ahigh public and policy profile, it’s theeffects of excess nutrients on bodies ofwater, especially in coastal areas. “Becauseof its high solubility, nitrate quickly escapesto down below the root zone of an agricul-tural field or forest and into groundwater,”says Donald Boesch, a professor of marinescience and president of the University of

Maryland’s Center for EnvironmentalScience. “That makes it difficult andexpensive to control.”

Reactive nitrogen—whether from ani-mal-raising facilities, manufactured fertiliz-er, septic systems, or other sources—hasraised nitrate concentrations in the water-ways of most industrialized nations. InNorway, nitrate concentrations in 1,000lakes doubled in less than a decade. Riversin the northeastern United States and inmuch of Europe have increased 10- to 15-fold in the last 100 years.

Where nitrate loading to bays andcostal zones increases (rivers tend to be lessaffected), it can provide such a steadysource of nutrients that algae bloom uncon-trollably. When the algae die, they sink anddecompose, which draws oxygen from thewater. If too much oxygen is removed, thewater body develops a “dead zone”—anarea that can no longer support finfish,shellfish, or most other aquatic life. Perhapsthe best-known dead zone is that found inthe Gulf of Mexico, which is fed by thenitrate-rich Mississippi River and fluctuatesin size from 3,000 to 8,000 square miles.There are also oxygen-starved areas in theBaltic Sea, the Adriatic Sea, the Gulfof Thailand, the Yellow Sea, and theChesapeake Bay.

Boesch notes that scientists were sayingas far back as 1987 that 40% of the nitro-gen coming into the system needed to beremoved. But so far, he says, programs toreduce reactive nitrogen in the ChesapeakeBay haven’t significantly improved the bay’s

health. And although rivers are generallyless susceptible to such algal blooms andoxygen losses, Mallin has found similareffects in North Carolina’s blackwaterstreams, so called because they are rich inorganic matter. “Regardless of what we add[nitrate, ammonia, or urea from livestock],it will stimulate algae growth in these black-water streams,” he says.

Reactive nitrogen can also infiltratedrinking water, as nitrates from nitrogenfertilizers and runoff from livestock findtheir way into streams, rivers, lakes, andgroundwater. In the United States,Townsend says, as much as 20% of ground-water sources may exceed the U.S. andWorld Health Organization limits of 10parts per million for nitrates. This concen-tration is also exceeded in many other partsof the world. High concentrations ofnitrates can cause methemoglobinemia—or“blue baby disease”—in infants. In bluebaby disease, nitrate ions weaken theblood’s capacity to carry oxygen. Epide-miological studies have also linked nitratesto reproductive problems and some can-cers, including increased risks for bladderand ovarian cancers at concentrationsbelow 10 parts per million.

Nitrogen in the SoilAs with water and air, reactive nitrogenbuilds up in soil. There’s a limit, however,to how much nitrogen plants can use.When soil reaches a point at which plantscan’t use additional nitrogen, it’s said to be“saturated.” And saturated soil, in theory at

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School of hard NOx. Burning of biomass and combustion of fossil fuels both produce NOx, a sig-nificant contributor to the formation of smog and ground-level ozone.

least, will shed any additional nitrogenintroduced to it. But that nitrogen doesn’tleave unaccompanied. “When it leaches outof the system,” says Townsend, “it takesother nutrients with it, so it ends up acidi-fying the soil, and it takes things like mag-nesium and calcium out into the water.And you end up with a very unbalancedsystem.”

If it’s true that saturated soil immediate-ly passes additional nitrogen, rather thandenitrifying it, that could be bad news forthe near future, says Howarth, with all thatexcess nitrogen flowing straight to ground-water, rivers, streams, and seas. However, hesays, we have a very poor understanding ofwhat is actually happening. “If the nitrogenis accumulating in soil, it could be a tem-porary phenomenon until it saturates theability to store it. Then we have a muchbigger problem,” he says. “If it is being de-nitrified, on the other hand, that’s more ofa steady-state process, and it can probablycontinue to do that.”

Townsend says some scientists hadhoped that excess reactive nitrogen levelsmight actually reduce greenhouse gases bystimulating plant growth, which locks upcarbon dioxide. But, he says, “It doesn’tseem likely that it’s going to play a domi-nant role.” Although the jury is still out,Tilman adds, “there isn’t very good evidencethat nitrogen deposition actually does leadto increased carbon removal and storage.”

Although more reac-tive nitrogen means moregrowth, it also changeswhich of the species in anecosystem thrive. Forexample, in grasslands thatreceived increased nitrogen,Tilman says, “the speciescomposition changed toplants that had litter thatdecomposed more quickly.And because it decom-posed more quickly, therewas actually no net storageof carbon with addednitrogen.”

On the surface it couldseem as though additionalnutrition might at leasthelp struggling ecosystemsthrive. In fact, however,reactive nitrogen can dis-rupt an ecosystem’s deli-cate balance. “From the1850s on, we’ve knownthat the addition of nutri-ents to terrestrial ecosys-tems causes changes inwhich species are thereand causes a loss of diver-

sity in those systems,” says Tilman.“Under the highest rates of agriculturallydriven nitrogen that we’ve seen, there’s avery strong effect [on biodiversity loss].”Recent field studies in Great Britain—

reported by Open University Earth scientistCarly J. Stevens and colleagues in the 19March 2004 issue of Science—have con-firmed that biodiversity decreased as unaid-ed nitrogen deposition increased in a sam-ple of 68 grasslands. Tilman’s experimentalwork in which nitrogen was added toecosystems shows similar results, he says.

Regaining ControlReducing the amount of reactive nitrogenthat is added to the environment is critical,Galloway says. Of the nitrogen that is creat-ed to sustain food production, only about2–10% enters the human mouth, dependingon the region. The rest, he says, is lost to theenvironment: “Unless an equivalent amountis denitrified back to molecular N2, then thatmeans reactive nitrogen is accumulating inthe environment, in the atmosphere, in thegroundwater, in the soils, in the biota.”

Some solutions are at best long-term,or simply unlikely. If many of the world’smeat-eaters were to switch to a largely veg-etarian diet, Townsend says, farmers couldplant far less nitrogen-stoked grain, mostof which goes to animal feed and sweeten-ers. But meat consumption in the UnitedStates and Asia is rising rather than falling.It has also been suggested that symbioticbacteria could someday be genetically engi-neered to bestow grains directly with nitro-gen-fixing capability.

A more practical, low-tech, low-costsolution is to improve the ways farmers


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A rising tide. Nitrogen fertilizer runoff contributes to the forma-tion of algal blooms such as this red tide bloom, which extendedmore than 100 miles along Florida’s Gulf coastline in 2001. Suchblooms kill thousands of fish and threaten human health.

Source: Lambert KF, Driscoll C. 2003. Nitrogen Pollution: From the Sources to the Sea. Hanover, NH: Hubbard Brook Research Foundation; 6.


rotate crops and fertilize their lands, saysStanford University Earth science profes-sor Pamela Matson. In the AmericanMidwest, for example, it’s common forfarmers to fertilize their fields in the fall.Winter snow and spring thaw wash awayfar more fertilizer than stays in the soil.Many farmers in all regions that have espe-cially unpredictable weather intentionallyoverfertilize, she says, rather than run therisk of running short of nutrients in a yearin which conditions would otherwiseresult in a bumper crop. The alternative,which Matson says some farmers managewell, is to add exactly the right amount offertilizer exactly when it is needed.

In an effort to better understand theproblems associated with changes in thenitrogen cycle and reduce their negativeimpacts, the Swedish-based InternationalGeosphere–Biosphere Programme and theFrench-based Scientific Committee onProblems of the Environment have teamedup to support the International NitrogenInitiative (INI). This international projectis planned as a three-phase effort to assessthe state of the knowledge of nitrogen flowsand problems, develop region-specificstrategies, and put those strategies into

place, with regional centers to be estab-lished to carry out these goals. The INI willcosponsor the Third International NitrogenConference, scheduled for 12–16 October2004 in Nanjing, China. There, scientistswill focus on the problems specific to Asiaand examine options for increasing foodand energy production while reducingnitrogen pollution. During this meeting,the INI Scientific Advisory Committee willmeet to plan one or more regional centersfor Asia.

Ultimately, however, the answer is toregulate reactive nitrogen the same asother pollutants, Likens says. In Europe,regulations have helped reduce nitrogenpollution, Galloway says. But the UnitedStates—not to mention developingnations—has a long way to go, not just indeveloping regulations, but in understand-ing the dynamics of the nitrogen cycle,Galloway says.

He cites the example of federal regula-tions to reduce nitrogen losses from hogfarms. “A lagoon system was mandated todecrease reactive nitrogen–containing wasterelease into waters. The waste was stored inthese big lagoons and then aerated—whichreleased ammonia to the atmosphere—and

the sludge was spread onto fields to growcover crops,” he explains. The system worksinsofar as it keeps the nitrogen out of therivers fairly well. “But it just transfers [thenitrogen] to the atmosphere,” Gallowaysays. “You need to have an integrated man-agement policy.”

We know the global nitrogen system isbeing disrupted, Galloway says. “What wedon’t know is the rate that nitrogen is accu-mulating. And because reactive nitrogencontributes to many environmental issuesof the day, the more you have, the faster therate of accumulation, and the more you’regoing to have an increase in the effects anddistribution of the effects.”

“Humans are changing the nitrogencycle globally faster than any other majorbiogeochemical cycle—it’s just goingthrough the roof in a hurry,” Townsendsays. “The problems with that are remark-ably diverse and widespread, and we reallyneed to do something about it. But I thinkthe good news is that there are a lot of waysto envision that we could do somethingabout it without utterly turning socioeco-nomic systems on their ear.”

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Saturation point. Experts warn that nitrogen-saturated soilsmay not be able to keep the excess from the environment. Source: Lambert KF, Driscoll C. 2003. Nitrogen Pollution: From the Sources to the Sea. Hanover, NH: Hubbard Brook

Research Foundation; 16.

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