Human Alteration of the Global Nitrogen Cycle: Causes and Consequences
Human Alteration of the Global Nitrogen Cycle: Causes and Consequences Photo by Nadine Cavender I Published by the Ecological Society of America Number 1, Spring 1997 ssues in Eco logy
Issues in Ecology Number I Spring 1997 Human Alteration of the Global Nitrogen Cycle: Causes and Consequences SUMMARY Human activities are greatly increasing the amount of nitrogen cycling between the living world and the soil.water,and atmosphere.In fact,humans have already doubled the rate of nitrogen entering the land-based nitrogen cycle.and that rate is continuing to climb.This human-driven global change is having serious impacts on ecosystems around the world because nitrogen is essential to living organisms and its availability plays a crucial role in the organization and functioning of the world's ecosystems.In many eco osystems on land and sea,the supply of nitrogen is a key factor the unmanaged systems but in most croplands and forestry plantations as well.Excessive nitrogen additions can pollute ecosystems 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 use of nitrogen fertilizers to the buming of fossil fuels in automobiles.power generation plants.and industries.However human activities have not eased the through air and w ause of this inc ty,ex nitrogen from human 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 (N).a potent greenhouse gas.in the atmosphere as vell as in nitrogen (including nitric oxide.NO)that drive the formation of photo ical 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.and subsequently.the animals and microbes that depend on these plants: Caused changes in the plant and animal life and ecological processes of estuarine and nearshore ecosystems,and contributed to long-term declines in coastal marine fisheries. titetothe impt through the developmentand fam management practices that burgeoning demand for and release of nitrogenous fertilizers
SUMMARY Human activities are greatly increasing the amount of nitrogen cycling between the living world and the soil, water, and atmosphere. In fact, humans have already doubled the rate of nitrogen entering the land-based nitrogen cycle, and that rate is continuing to climb. This human-driven global change is having serious impacts on ecosystems around the world because nitrogen is essential to living organisms and its availability plays a crucial role in the organization and functioning of the worlds ecosystems. In many ecosystems on land and sea, the supply of nitrogen is a key factor controlling the nature and diversity of plant life, the population dynamics of both grazing animals and their predators, and vital ecological processes such as plant productivity and the cycling of carbon and soil minerals. This is true not only in wild or unmanaged systems but in most croplands and forestry plantations as well. Excessive nitrogen additions can pollute ecosystems 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 use of 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 nitrogen through air and water. Because of this increased mobility, excess nitrogen from human activities has serious and longterm 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 (N2 O), a potent greenhouse gas, in the atmosphere as well as increased regional concentrations of other oxides of nitrogen (including nitric oxide, NO) that drive 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, and subsequently, the animals and microbes that depend on these plants; • Caused changes in the plant and animal life and ecological processes of estuarine and nearshore ecosystems, and contributed to long-term declines in coastal marine fisheries. National and international policies should attempt to reduce these impacts through the development and widespread dissemination of more efficient fossil fuel combustion technologies and farm management practices that reduce the burgeoning demand for and release of nitrogenous fertilizers. Human Alteration of the Global Nitrogen Cycle: Causes and Consequences Issues in Ecology Number 1 Spring 1997 2
Issues in Ecology Number I Spring 1997 Human Alteration of the Global Nitrogen Cycle: Causes and Consequences Gene E.Likens.PamelaAMatson,David W.Schindler. William H.Schlesinger,and G.David Tilman INTRODUCTION factors that the dy namics, f many ecosystems This report presents an overview of the current The Earth's atmosphere is 78 percent nitrogen scientific understanding of human-driven changes to the gas,but most plants and animals cannot use nitrogen global nitrogen cycle and their consequences.It also gas directly from the air as they do carbon dioxide and addresses policy and management options that could help oxygen.Instead,plants-and all organisms from the moderate these changes in the nitrogen cycle and their impacts. aaa山 ely secur thei from the synth zed by pla must wait THE NITROGEN CYCLE to hydrogen or oxygen to form inorganic compounds Nitrogen is an essential component of proteins. mainly ammonium (NH,)and nitrate (NO,).that they genetic material,chlorophyll.and other key organic mol can use r to live.It The amount of gaseous nitrogen being fixed at nd hyd t inliving tiss bd any e bv ts only human activities began to alter the natural cycle(Figure that cycles among the living and nonliving components 1).however,nitrogen was only scantily available to much of the Earth's ecosystems.Most of that nitrogen,too. of the biological world.As a result,nitrogen served as is unavailable,locked up in soil organic matter-par- Atmospheric nitrogen Amino acid NO and NH soll wat by Saders Collse ns d Ad apted from Environmental Science Third Edition by Jonathon 2
INTRODUCTION This report presents an overview of the current scientific understanding of human-driven changes to the global nitrogen cycle and their consequences. It also addresses policy and management options that could help moderate these changes in the nitrogen cycle and their impacts. THE NITROGEN CYCLE Nitrogen is an essential component of proteins, genetic material, chlorophyll, and other key organic molecules. All organisms require nitrogen in order to live. It ranks fourth behind oxygen, carbon, and hydrogen as the most common chemical element in living tissues. Until human activities began to alter the natural cycle (Figure 1), however, nitrogen was only scantily available to much of the biological world. As a result, nitrogen served as 1 Human Alteration of the Global Nitrogen Cycle: Causes and Consequences by Peter 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 dynamics, biodiversity, and functioning of many ecosystems. The Earths atmosphere is 78 percent nitrogen gas, but most plants and animals cannot use nitrogen gas directly from the air as they do carbon dioxide and oxygen. Instead, plants and all organisms from the grazing animals to the predators to the decomposers that ultimately secure their nourishment from the organic materials synthesized by plants must wait for nitrogen to be fixed, that is, pulled from the air and bonded to hydrogen or oxygen to form inorganic compounds, mainly ammonium (NH4 ) and nitrate (NO3 ), that they can use. The amount of gaseous nitrogen being fixed at any given time by natural processes represents only a small addition to the pool of previously fixed nitrogen that cycles among the living and nonliving components of the Earths ecosystems. Most of that nitrogen, too, is unavailable, locked up in soil organic matter parFigure 1-Simplified diagram of the nitrogen cycle. Adapted from Environmental Science, Third Edition by Jonathon Turk and Amos Turk, 81984 by Saunders College Publishing, reproduced by permission of the publisher. 3 Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 tially rotted plant and animal remains-that must be a million metric tons of nitrogen.Worldwide.lightning decomposed by soil microbes. release for nst ce cycled through the food web.The two major natural natural suppliers of new biologically available nitrogen. sources of new nitrogen entering this cycle are nitrogen- Before the widespread planting of legume crops.terres fixing organisms and lightning. trial organisms probably fixed between 90 and 140 Tg Nitrogen-fixing organisms include a relatively of nitrogen per vear.a reasonable upper bound for the small number of algae and bacteria.Many of them live rate of natural nitrogen fixation on land is thus about 140 Tg of N per year Symbiotic nitrogen-fixing bacteria such as the Rhizobia, HUMAN-DRIVEN NITROGEN FIXATION for instance.live and work in nodules on the roots of peas,beans,alfalfa and other legumes.These bacteria During the past century,human activities clearly have accelerated the rate of nitrogen fixation on land effectively doubling the annual transfer of nitrogen from Lightning ma tly transform atmo the vast av lable atr spher ic pool to the biolog spheric nitrogen into itrates.which rain onto soil. cally available forms.The major sources of this enhance Quantifying the rate of natural nitrogen fixation supply include industrial processes that produce nitro prior to human alterations of the cycle is difficult but gen fertilizers.the combustion of fossil fuels,and the necessary for evaluating the impacts of human-driven cultivation of soybeans,peas,and other crops that host changes to the global cycling of nitrogen.The standard symbiotic nitrogen-fixing bacteria.Furthermore,human ctivity is also speeding up the release of nitrogen from g).which is equal to long-term storage in soi organic matter Figure 2-Nitrogen is the major factor limiting many terrestrial ecosystems.including most of those in the temperate zone,such as this oak savannah.The number and identities of the plant and animal species that live in such terrestrial ecosystems,and the functioning of the ecosystem,depends on the rate of nitrogen supply to the ecosystem
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 major natural suppliers of new biologically available nitrogen. Before the widespread planting of legume crops, terrestrial organisms probably fixed between 90 and 140 Tg of nitrogen per year. A reasonable upper bound for the rate of natural nitrogen fixation on land is thus about 140 Tg of N per year. HUMAN-DRIVEN NITROGEN FIXATION During the past century, human activities clearly have accelerated the rate of nitrogen fixation on land, effectively doubling the annual transfer of nitrogen from the vast but unavailable atmospheric pool to the biologically available forms. The major sources of this enhanced supply include industrial processes that produce nitrogen fertilizers, the combustion of fossil fuels, and the cultivation of soybeans, peas, and other crops that host symbiotic nitrogen-fixing bacteria. Furthermore, human activity is also speeding up the release of nitrogen from long-term storage in soils and organic matter. tially rotted plant and animal remains that must be decomposed by soil microbes. These microbes release nitrogen as ammonium or nitrate, allowing it to be recycled through the food web. The two major natural sources of new nitrogen entering this cycle are nitrogenfixing organisms and lightning. Nitrogen-fixing organisms include a relatively small number of algae and bacteria. Many of them live free in the soil, but the most important ones are bacteria that 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 of peas, beans, alfalfa and other legumes. These bacteria manufacture an enzyme that enables them to convert gaseous nitrogen directly into plant-usable forms. Lightning may also indirectly transform atmospheric nitrogen into nitrates, which rain onto soil. Quantifying the rate of natural nitrogen fixation prior to human alterations of the cycle is difficult but necessary for evaluating the impacts of human-driven changes to the global cycling of nitrogen. The standard unit of measurement for analyzing the global nitrogen cycle is the teragram (abbreviated Tg), which is equal to 4 Figure 2-Nitrogen is the major factor limiting many terrestrial ecosystems, including most of those in the temperate zone, such as this oak savannah. The number and identities of the plant and animal species that live in such terrestrial ecosystems, and the functioning of the ecosystem, depends on the rate of nitrogen supply to the ecosystem. Photo by D. Tilman Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 Sources of Human-Caused Alteration to the Global Nitrogen Cycle Figure 3-The pace of many hu man-caused global changes has increased starkly in modern his- 75 tory,but none so rapidly as in dustria pr .Deforestation f nitrogen fertiliz .CO.release ponentially since the 1940 509% Human population The chart shows the vear which changes in human population growth carbon dioxide release deforestation.and fertilizer pro 25% duction had r reached25% and 759 the exten 1700 1800 1900 107 50 seen in the late 190s Revised from Kates et al.(1990). Nitrogen Fertilizer nitrogen directly from the atmosphere and greatly in ndustrial fixation of nitrogenfor use as fertilizer crease the rate of nitrogen f ation previously occurring currently totals approximately 80 Tg per year and repre- on those lands. Substantial levels of nitrogen fixation sents by far the largest human contribution of new nitro also occur during cultivation of some non-legumes,nota gen to the global cycle (Figure 3).That figure does not bly rice.All of this represents new,human-generated etatansterofaheayfiag stocks of biologically available nitrogen.The quantity of which r rogen fron nitrog crop difficult to ana e tha one o anothe tha new ind duction Estim e from 32 The process of manufacturing fertilizer by indus rial nitrogen pro to 53 Tg per year.As an average.40 Tg will be used trial nitrogen fixation was first developed in Germany here. during world War l.and fertilizer production has grown exponentially since the 1940s.In recent years,the in- Fossil Fuel Burning creasing pace of production and use has been truly phe The burning of fossil fuels such as coal and oil nomenal.The unt of industrially fixed nit releases fixed nitrog lon -te stor the decade f m1980019960 age in geol al for ck to the osphere more than equaled all i industrial fertilizer applied previ the form of nitrogen-base ed trace gases such as nitr ously in human history. oxide.High-temperature combustion also fixes a sma Until the late 1970s,most industrially produced amount of atmospheric nitrogen directly.Altogether,the fertilizer was applied in developed countries.Use in these operations of automobiles,factories,power plants,and regions has now stabilized while fertilizer applications in other combustion processes emit more than 20 Tg per developing countries have risen dramatically.The mo year of fixed nitrogen to the atmosphere. All of it is of human popu h a and inc ated her s wly fixed se it has bee zation ens es t locked up for ns of years and would remain locke continue at high and likely accelerating rates for decades up indefinitely if not released by human action. in order to meet the escalating demand for food. Mobilization of stored nitrogen Nitrogen-Fixing Crops Besides enhancing fixation and releasing nitro Nearly one third of the Earth's land surface is gen from geological reservoirs.hur man activities also lib ultural and astoral uses and human genfomlongermbiologtcalstorag have replaced large areas of diverse natural vegetatior such as soil organ c matter an uting with monocultures of soybeans,peas,alfalfa,and other further to the proliferation of biologically available nitro leguminous crops and forages.Because these plants sup gen.These activities include the burning of forests,wood port symbiotic nitrogen-fixers,they derive much of their fuels,and grasslands,which emits more than 40 Tg per
5 Nitrogen Fertilizer Industrial fixation of nitrogen for use as fertilizer currently totals approximately 80 Tg per year and represents by far the largest human contribution of new nitrogen to the global cycle (Figure 3). That figure does not include manures and other organic nitrogen fertilizers, which represent a transfer of already-fixed nitrogen from one place to another rather than new fixation. The process of manufacturing fertilizer by industrial nitrogen fixation was first developed in Germany during World War I, and fertilizer production has grown exponentially since the 1940s. In recent years, the increasing pace of production and use has been truly phenomenal. The amount of industrially fixed nitrogen applied to crops during the decade from 1980 to 1990 more than equaled all industrial fertilizer applied previously in human history. Until the late 1970s, most industrially produced fertilizer was applied in developed countries. Use in these regions has now stabilized while fertilizer applications in developing countries have risen dramatically. The momentum of human population growth and increasing urbanization ensures that industrial fertilizer production will continue at high and likely accelerating rates for decades in order to meet the escalating demand for food. Nitrogen-Fixing Crops Nearly one third of the Earths land surface is devoted to agricultural and pastoral uses, and humans have replaced large areas of diverse natural vegetation with monocultures of soybeans, peas, alfalfa, and other leguminous crops and forages. Because these plants support symbiotic nitrogen-fixers, they derive much of their nitrogen directly from the atmosphere and greatly increase the rate of nitrogen fixation previously occurring on those lands. Substantial levels of nitrogen fixation also occur during cultivation of some non-legumes, notably rice. All of this represents new, human-generated stocks of biologically available nitrogen. The quantity of nitrogen fixed by crops is more difficult to analyze than industrial nitrogen production. Estimates range from 32 to 53 Tg per year. As an average, 40 Tg will be used here. Fossil Fuel Burning The burning of fossil fuels such as coal and oil releases previously fixed nitrogen from long-term storage in geological formations back to the atmosphere in the form of nitrogen-based trace gases such as nitric oxide. High-temperature combustion also fixes a small amount of atmospheric nitrogen directly. Altogether, the operations of automobiles, factories, power plants, and other combustion processes emit more than 20 Tg per year of fixed nitrogen to the atmosphere. All of it is treated here as newly fixed nitrogen because it has been locked up for millions of years and would remain locked up indefinitely if not released by human action. Mobilization of Stored Nitrogen Besides enhancing fixation and releasing nitrogen from geological reservoirs, human activities also liberate nitrogen from long-term biological storage pools such as soil organic matter and tree trunks, contributing further to the proliferation of biologically available nitrogen. These activities include the burning of forests, wood fuels, and grasslands, which emits more than 40 Tg per Figure 3-The pace of many human-caused global changes has increased starkly in modern history, but none so rapidly as industrial production of nitrogen fertilizer, which has grown exponentially since the 1940s. The chart shows the year which changes in human population growth, carbon dioxide release, deforestation, and fertilizer production had reached 25%, 50%, and 75% of the extent seen in the late 1980s. Revised from Kates et al. (1990). 25% 50% 75% 1700 1800 1900 1975 Deforestation CO release 2 Human population Industrial N fertilizer Sources of Human-Caused Alteration to the Global Nitrogen Cycle Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 year of nitrogen:the draining of wetlands.which sets all of the more than 20 Tg per year of fixed nitroge the idation of so organic matter that released in bile exha in emission nitrogen:and land from foss burning is emitted to o the atmosphere as clearing for crops,which could mobilize 20 Tg per year nitric oxide.Other activities indirectly enhance emissions from soils. to the atmosphere.Intensive fertilization of agricultural There are substantial scientific uncertainties about soils can increase the rates at which nitrogen in the form both the quantity and the fate of nitrogen mobilized by of ammonia is volatilized and lost to the air.It can also such activities.Taken together.however.they could con changes in the enha ncin the Ever cycle. runmanaged lands downwind of agri industrial areas,rain or windborne deposition of human Human Versus Natural Nitrogen Fixation generated nitrogen can spur increased emissions of ni Overall,fertilizer production.legume crops.and trogen gases from the soils. fossil fuel burning deposit approximately 140 Tg of new aogcnintolhndbasedecosystemseacthyear'afigure Nitrous Oxide that quals the pe rog n fixed na Nitrous xide isa very heat-trapping rally by organisms se ecosystem Other huma gas in the nosphere.in part because it absorbs activities liberate and make available half again that much ing radiant heat from the Earth in infrared wavelengths nitrogen.From this evidence,it is fair to conclude that that are not captured by the other major greenhouse human activities have at least doubled the transfer of gases,water vapor and carbon dioxide.By absorbing nitrogen from the atmosphere into the land-based bio and reradiating this heat back toward the farth.nitrous oxide contributes a few percent to overall greenhouse trogen is spread unev nly across the warmin Earth's surface: me area n as northe ern Europe are Although nitro oxide is unread tive and long lived in the lower atmosphere,when it rises into the strato gions in the Southern Hemisphere receive little direct in- sphere it can trigger reactions that deplete and thin the put of human-generated nitrogen.Yet no region remains stratospheric ozone layer that shields the Earth from unaffected.The increase in fixed nitrogen circulating damaging ultraviolet radiation. The concentration of nitrous oxide in the atmo ,even in cores drilled sphere e is curre ntly i ncr reasing at the rate of to th the glacia ice nd tenths of a percent per yea that d,the sources of the increase remain unre IMPACTS ON THE ATMOSPHERE solved.Both fossil fuel burning and the direct impacts of agricultural fertilization have been considered and re One major consequence of human-driven alter. jected as the major source.Rather.there is a developins ations in the nitrogen cycle has been regionl and global consensus that a wide array of human-driven sources change in the che of the atmos ntribute ically to ich the te strial nitr specifically.increased ons gen cycle. “disper rsed sources incl de gases such as nitrous oxide,nitric oxide,and ammonia nitrogen-enriched ground ater,nitrogen-saturated for (NH,).Although such releases have received less atten ests,forest burning.land clearing.and even the manu tion than increased emissions of carbon dioxide and vari- facture of nylon.nitric acid.and other industrial prod ous sulfur compounds.the trace nitrogen gases cause ucts. environmental effects both while airbome and after they The net effect is increased global concentrations ited on theground.For instan of a poter that also contributes to the long-lived in t e atmosp ere and ozone layer human-driven enhancement of the greenhouse effect that likely warms the Earth's climate.Nitric oxide is an im- Nitric Oxide and Ammonia portant precursor of acid rain and photochemical smog. Unlike nitrous oxide.which is unreactive in the Some of the human activities discussed above lower atmosphere,both nitric oxide and ammonia are affect the atmosphere directly.For instance,essentially highly reactive and therefore much shorter lived.Thus
year of nitrogen; the draining of wetlands, which sets the stage for oxidation of soil organic matter that could mobilize 10 Tg per year or more of nitrogen; and land clearing for crops, which could mobilize 20 Tg per year from soils. There are substantial scientific uncertainties about both the quantity and the fate of nitrogen mobilized by such activities. Taken together, however, they could contribute significantly to changes in the global nitrogen cycle. Human Versus Natural Nitrogen Fixation Overall, fertilizer production, legume crops, and fossil fuel burning deposit approximately 140 Tg of new nitrogen into land-based ecosystems each year, a figure that equals the upper estimates for nitrogen fixed naturally by organisms in these ecosystems. Other human activities liberate and make available half again that much nitrogen. From this evidence, it is fair to conclude that human activities have at least doubled the transfer of nitrogen from the atmosphere into the land-based biological nitrogen cycle. This extra nitrogen is spread unevenly across the Earths surface: Some areas such as northern Europe are being altered profoundly while others such as remote regions in the Southern Hemisphere receive little direct input of human-generated nitrogen. Yet no region remains unaffected. The increase in fixed nitrogen circulating around the globe and falling to the ground as wet or dry deposition is readily detectable, even in cores drilled from the glacial ice of Greenland. IMPACTS ON THE ATMOSPHERE One major consequence of human-driven alterations in the nitrogen cycle has been regional and global change in the chemistry of the atmosphere (Figure 4) specifically, increased emissions of nitrogen-based trace gases such as nitrous oxide, nitric oxide, and ammonia (NH3). Although such releases have received less attention than increased emissions of carbon dioxide and various sulfur compounds, the trace nitrogen gases cause environmental effects both while airborne and after they are deposited on the ground. For instance, nitrous oxide is long-lived in the atmosphere and contributes to the human-driven enhancement of the greenhouse effect that likely warms the Earths climate. Nitric oxide is an important precursor of acid rain and photochemical smog. Some of the human activities discussed above affect the atmosphere directly. For instance, essentially all of the more than 20 Tg per year of fixed nitrogen released in automobile exhausts and in other emissions from fossil fuel burning is emitted to the atmosphere as nitric oxide. Other activities indirectly enhance emissions to the atmosphere. Intensive fertilization of agricultural soils can increase the rates at which nitrogen in the form of ammonia is volatilized and lost to the air. It can also speed the microbial breakdown of ammonium and nitrates in the soil, enhancing the release of nitrous oxide. Even in wild or unmanaged lands downwind of agricultural or industrial areas, rain or windborne deposition of humangenerated nitrogen can spur increased emissions of nitrogen gases from the soils. Nitrous Oxide Nitrous oxide is a very effective heat-trapping gas in the atmosphere, in part because it absorbs outgoing radiant heat from the Earth in infrared wavelengths that are not captured by the other major greenhouse gases, water vapor and carbon dioxide. By absorbing and reradiating this heat back toward the Earth, nitrous oxide contributes a few percent to overall greenhouse warming. Although nitrous oxide is unreactive and longlived in the lower atmosphere, when it rises into the stratosphere it can trigger reactions that deplete and thin the stratospheric ozone layer that shields the Earth from damaging ultraviolet radiation. The concentration of nitrous oxide in the atmosphere is currently increasing at the rate of two- to threetenths of a percent per year. While that rise is clearly documented, the sources of the increase remain unresolved. Both fossil fuel burning and the direct impacts of agricultural fertilization have been considered and rejected as the major source. Rather, there is a developing consensus that a wide array of human-driven sources contribute systematically to enrich the terrestrial nitrogen cycle. These dispersed sources include fertilizers, nitrogen-enriched groundwater, nitrogen-saturated forests, forest burning, land clearing, and even the manufacture of nylon, nitric acid, and other industrial products. The net effect is increased global concentrations of a potent greenhouse gas that also contributes to the thinning of the stratospheric ozone layer. Nitric Oxide and Ammonia Unlike nitrous oxide, which is unreactive in the lower atmosphere, both nitric oxide and ammonia are highly reactive and therefore much shorter lived. Thus 6 Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 Human-Caused Global Nitrogen Emissions 100% Figure 4-Human for large f trogen-containing trace gases,including 40% of the nitrous oxide,80%or more of nitric ox- ide.and 70%of ammonia releases.the result is increasing atmospheric concentrations of the og,andofbiologicalyavailabte from the atm sphere to fertil ize ecosystems Ammonia data are from Schlesinger and Hartley (1992).nitric oxide from Delmas et al.(in press).and nitrous oxide from Prather et al.(1995). (NH) (NO) (N.O) changes in their atmospheric concentrations can be de- EFFECTS ON THE CARBON CYCLE tected only at local or regional scales. Nitric oxide plays several critical roles in atmo- Increased emissions of airborne nitrogen have led spheric chemistry,including catalyzing the formation of to enhanced deposition of nitrogen on land and in the photochemical (or brown)smog.In the presence of sun oceans.Thanks to the fertilizer effects of nitrogen in light,nitric oxide and react with hydrocarb may be e.the most atmospherei dir ty by altering the g bal carbon cycle. serious detrimental effects on human health as well as Over much of the Earth's surface,the lushness the health and productivity of crops and forests. of plant growth and the accumulation of standing stocks Nitric oxide.along with other oxides of nitrogen of plant material historically have been limited by scanty and sulfur,can be transformed in the atmosphere into nitrogen supplies,particularly in temperate and boreal aio compo regions.Hur an activity has substa tially ased the depositio a.whichraisc Although a number of sources contribute toni mroHow mro tric oxide emissions,combustion is the dominant one been caused by human-generated nitrogen additions?As Fossil fuel burning emits more than 20 Tg per year of a result.how much extra carbon has been stored in ter nitric oxide.Human burning of forests and other plant restrial ecosystems rather than contributing to the rising material may add about 10 Tg,and global emissions of concentrations of carbon dioxide in the atmosphere? nitric oxide from soils.a substantial fraction of which are Answers to these questions could help explain ,year al,80 the imbalance i in the car。 that has co e to be percent o more of nitric ide emr known as the ing sink. know generated by human activities.and in many regions the carbon dioxide from human activities such as fossil fue result is increased smog and acid rain. burning and deforestation exceed by more than 1,00C In contrast to nitric oxide,ammonia acts as the Tg the amount of carbon dioxide known to be accumu primary acid-neutralizing agent in the atmosphere.hav lating in the atmosphere each year.Could increased ing an opposite influence on the acidity of aerosols growth rates in terrestrial vegetation be thesinktha and rainfall.Nearly 70 per accounts for the fate of much oftha mis ammonia emissions are human-caused Experiments in Europe and America indicate tha tilized from fertilized fields contributes an estimated 1 a large portion of the extra nitrogen retained by forest Tg per year:ammonia released from domestic animal wetland,and tundra ecosystems stimulates carbon up wastes about 32 Tg:and forest burning some 5 Tg. take and storage.On the other hand,this nitrogen can
EFFECTS ON THE CARBON CYCLE Increased emissions of airborne nitrogen have led to enhanced deposition of nitrogen on land and in the oceans. Thanks to the fertilizer effects of nitrogen in stimulating plant growth, this deposition may be acting to influence the atmosphere indirectly by altering the global carbon cycle. Over much of the Earths surface, the lushness of plant growth and the accumulation of standing stocks of plant material historically have been limited by scanty nitrogen supplies, particularly in temperate and boreal regions. Human activity has substantially increased the deposition of nitrogen over much of this area, which raises important questions: How much extra plant growth has been caused by human-generated nitrogen additions? As a result, how much extra carbon has been stored in terrestrial ecosystems rather than contributing to the rising concentrations of carbon dioxide in the atmosphere? Answers to these questions could help explain the imbalance in the carbon cycle that has come to be known as the missing sink. The known emissions of carbon dioxide from human activities such as fossil fuel burning and deforestation exceed by more than 1,000 Tg the amount of carbon dioxide known to be accumulating in the atmosphere each year. Could increased growth rates in terrestrial vegetation be the sink that accounts for the fate of much of that missing carbon? Experiments in Europe and America indicate that a large portion of the extra nitrogen retained by forest, wetland, and tundra ecosystems stimulates carbon uptake and storage. On the other hand, this nitrogen can changes in their atmospheric concentrations can be detected only at local or regional scales. Nitric oxide plays several critical roles in atmospheric chemistry, including catalyzing the formation of photochemical (or brown) smog. In the presence of sunlight, nitric oxide and oxygen react with hydrocarbons emitted by automobile exhausts to form ozone, the most dangerous component of smog. Ground-level ozone has serious detrimental effects on human health as well as the health and productivity of crops and forests. Nitric oxide, along with other oxides of nitrogen and sulfur, can be transformed in the atmosphere into nitric acid and sulfuric acid, which are the major components of acid rain. Although a number of sources contribute to nitric oxide emissions, combustion is the dominant one. Fossil fuel burning emits more than 20 Tg per year of nitric oxide. Human burning of forests and other plant material may add about 10 Tg, and global emissions of nitric oxide from soils, a substantial fraction of which are human-caused, total 5 to 20 Tg per year. Overall, 80 percent or more of nitric oxide emissions worldwide are generated by human activities, and in many regions the result is increased smog and acid rain. In contrast to nitric oxide, ammonia acts as the primary acid-neutralizing agent in the atmosphere, having an opposite influence on the acidity of aerosols, cloudwater, and rainfall. Nearly 70 percent of global ammonia emissions are human-caused. Ammonia volatilized from fertilized fields contributes an estimated 10 Tg per year; ammonia released from domestic animal wastes about 32 Tg; and forest burning some 5 Tg. 7 Figure 4-Human activities are responsible for a large proportion of the global emissions of nitrogen-containing trace gases, including 40% of the nitrous oxide, 80% or more of nitric oxide, and 70% of ammonia releases. The result is increasing atmospheric concentrations of the greenhouse gas nitrous oxide, of the nitrogen precursors of smog, and of biologically available nitrogen that falls from the atmosphere to fertilize ecosystems. Ammonia data are from Schlesinger and Hartley (1992), nitric oxide from Delmas et al. (in press), and nitrous oxide from Prather et al. (1995). Issues in Ecology Number 1 Spring 1997 Ammonia (NH )3 Nitric oxide (NO) Nitrous oxide (N O) 2 20% 40% 60% 80% 100% Human-Caused Global Nitrogen Emissions
Issues in Ecology Number I Spring 1997 also stimulate microbial decon tems.These impacts first be a rope On balance,however,the car observed significant increases in bon uptake through new plant nitrate concentrations in some growth appears to exceed the lakes and streams and also ex carbon losses.especially in for- tensive yellowing and loss of ests. needles in spruce and other co nifer forests subjectedto heav nitrogen depo sition amount of carbon that could b servations led to several fieldex stored in terrestrial vegetation periments in the U.S.and Eu thanks to plant growth spurred rope that have revealed a com by added nitrogen.The result- plex cascade of effects set in ing estimates range from 100 motion by excess nitrogen in for r.The num est As ammonium builds up more recent analyses as the in the soil,it is increasingly con magnitude of human-driver verted to nitrate by bacterial changes in the nitrogen cycle action.a process that releases has become clearer the most hydrogen ions and helps acidify recent analysis of the global Figure 5-ild plants living in natural ecosyste plant.domi the soil.The buildup of nitrat carbo mental py cle by such as this lupine.a nit nated the en-fixing nces nitrogen cycle for emiss ons of nitrou on C ides fro the soil so en concluded that nitrogen depo courages leaching of highly wa fuels,and intensive cultivation of legume crops now sition could represent a major ter-soluble nitrate into streams component of the missing car- adds as much nitrogen to terrestrial ecosystems as or groundwater.as these nega bon sink. do all natural processes combined. tively charged nitrates seep More precise estimates will become possible when away,they carry with them positively charged alkaline we have a mor complete understanding the fract erals such as magne ium,and of human-genera i ogen that actually is retaine an modifica ior within various land-based ecosystems. soil fertility by greatly accelerating the loss of calcium and other nutrients that are vital for plant growth.As NITROGEN SATURATION AND calcium is depleted and the soil acidified.aluminum ions ECOSYSTEM FUNCTIONING are mobilized,eventually reaching toxic concentrations that can damage tree roots or kill fish if the aluminum tgrowth washes into streams. Tree owing in soils replete with be incr atio some point nitrogen bu tarved of cal magne ium.and potas when the natural nitrogen deficiencies in an ecosystem sium can develop nutrient imbalances in their roots and are fully relieved,plant growth becomes limited by spar leaves.This may reduce their photosynthetic rate and sity of other resources such as phosphorus,calcium.or efficiency.stunt their growth,and even increase tree water.When the vegetation can no longer respond to deaths. further additions of nitrogen,the ecosy stem reaches a Nitrogen saturation is much further advanced n saturatior e ecosys nsive areas or north Europe than in Nort em is ecause human-gener plants.and microbes cannot use or retain any more.al is several times greater the e than in even the most ex new nitrogen deposits will be dispersed to streams, tremely affected areas of North America.In the nitro groundwater,and the atmosphere. gen-saturated ecosystems of Europe.a substantial frac nitrogen saturation has a number of damaging tion of atmospheric nitrate deposits move from the land consequences for the health and functioning of ecosys into streams without ever being taken up by organisms
tems. These impacts first became apparent in Europe almost two decades ago when scientists observed significant increases in nitrate concentrations in some lakes and streams and also extensive yellowing and loss of needles in spruce and other conifer forests subjected to heavy nitrogen deposition. These observations led to several field experiments in the U.S. and Europe that have revealed a complex cascade of effects set in motion by excess nitrogen in forest soils. As ammonium builds up in the soil, it is increasingly converted to nitrate by bacterial action, a process that releases hydrogen ions and helps acidify the soil. The buildup of nitrate enhances emissions of nitrous oxides from the soil and also encourages leaching of highly water-soluble nitrate into streams or groundwater. As these negatively charged nitrates seep away, they carry with them positively charged alkaline minerals such as calcium, magnesium, and potassium. Thus human modifications to the nitrogen cycle decrease soil fertility by greatly accelerating the loss of calcium and other nutrients that are vital for plant growth. As calcium is depleted and the soil acidified, aluminum ions are mobilized, eventually reaching toxic concentrations that can damage tree roots or kill fish if the aluminum washes into streams. Trees growing in soils replete with nitrogen but starved of calcium, magnesium, and potassium can develop nutrient imbalances in their roots and leaves. This may reduce their photosynthetic rate and efficiency, stunt their growth, and even increase tree deaths. Nitrogen saturation is much further advanced over extensive areas of northern Europe than in North America because human-generated nitrogen deposition is several times greater there than in even the most extremely affected areas of North America. In the nitrogen-saturated ecosystems of Europe, a substantial fraction of atmospheric nitrate deposits move from the land into streams without ever being taken up by organisms also stimulate microbial decomposition and thus releases of carbon from soil organic matter. On balance, however, the carbon uptake through new plant growth appears to exceed the carbon losses, especially in forests. A number of groups have attempted to calculate the amount of carbon that could be stored in terrestrial vegetation thanks to plant growth spurred by added nitrogen. The resulting estimates range from 100 to 1,300 Tg per year. The number has tended to increase in more recent analyses as the magnitude of human-driven changes in the nitrogen cycle has become clearer. The most recent analysis of the global carbon cycle by the Intergovernmental Panel on Climate Change concluded that nitrogen deposition could represent a major component of the missing carbon sink. More precise estimates will become possible when we have a more complete understanding of the fraction of human-generated nitrogen that actually is retained within various land-based ecosystems. NITROGEN SATURATION AND ECOSYSTEM FUNCTIONING There are limits to how much plant growth can be increased by nitrogen fertilization. At some point, when the natural nitrogen deficiencies in an ecosystem are fully relieved, plant growth becomes limited by sparsity of other resources such as phosphorus, calcium, or water. When the vegetation can no longer respond to further additions of nitrogen, the ecosystem reaches a state described as nitrogen saturation. In theory, when an ecosystem is fully nitrogen-saturated and its soils, plants, and microbes cannot use or retain any more, all new nitrogen deposits will be dispersed to streams, groundwater, and the atmosphere. Nitrogen saturation has a number of damaging consequences for the health and functioning of ecosys- 8 Figure 5-Wild plants living in natural ecosystems, such as this lupine, a nitrogen-fixing plant, dominated the nitrogen cycle for millions of years. Human production of nitrogen fertilizer, burning of fossil fuels, and intensive cultivation of legume crops now adds as much nitrogen to terrestrial ecosystems as do all natural processes combined. Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 or playing a role in the biological cycle. this constraint.New supplies of nitrogen showered upon In contrast.in the northeastern U.S..increased these ecosystems can cause a dramatic shift in the domi leaching of nitrates from the sol and large shifts in the nant and marked reduction in rall sp entraliosintreeleaN es genera ally have b obs the few pant species daptedto only in certain types of forests. These include high-el evation sites that receive large nitrogen deposits and sites bors.In England,for example,nitrogen fertilizers ap with shallow soils containing few alkaline minerals to plied to experimental grasslands have led to increased buffer acidification.Elsewhere in the U.S.,the early stages dominance by a few nitrogen-responsive grasses and loss of nitrogen saturation have been seen in response to el- of many other plant species.At the highest fertilization evated nitr he number of plant spe s declined mor than five fold.In North America ductions ted by fertilization of grass Some forests have a very high capacity to retain lands in Minnesota and California(Figures 7.8.and 9) added nitrogen,particularly regrowing forests that have In formerly species-rich heathlands across Western Eu- been subjected to intense or repeated harvesting.an ac- rope.human-driven nitrogen deposition has been blamed tivity that usually causes severe nitrogen losses.Over for great osses of biodiversity in recent decades. all,the ability of a forest to retain nit og en depends on In the netherlands.high hu its potential fo furthe growth and the extent of its cur sityint sive livestock oper and ndustrie have rent nitrogen stocks.Thus,the impacts of nitrogen depo combined to generate the high t rates of nitrogen depo sition are tightly linked to other rapidly changing hu- sition in the world.One well-documented consequenc man-driven variables such as shifts in land use,climate, has been the conversion of species-rich heathlands to spe and atmospheric carbon dioxide and ozone levels. cies-poor grasslands and forest.Not only the species richness of the heath but also the biological diversity of EFFECTS ON BIODIVERSITY AND THE SPECIES MIX the lands has been reduced becaus the plant nities now resen ble the mpos on of com Limited supplies of biologically available nitrogen munities occupying more fertile soils.The unique species are a fact of life in most natural ecosystems,and many assemblage adapted to sandy,nitrogen-poor soils is be native plant species are adapted to function best under ing lost from the region. Figure 6-Deposition of nitrogen from the atmosphere is believed to be responsible for the vellow ing and loss of needles fro conifers and for ses of forest dieback.suck as that shown here 9
this constraint. New supplies of nitrogen showered upon these ecosystems can cause a dramatic shift in the dominant species and also a marked reduction in overall species diversity as the few plant species adapted to take full advantage of high nitrogen out compete their neighbors. In England, for example, nitrogen fertilizers applied to experimental grasslands have led to increased dominance by a few nitrogen-responsive grasses and loss of many other plant species. At the highest fertilization rate, the number of plant species declined more than fivefold. In North America, similarly dramatic reductions in biodiversity have been created by fertilization of grasslands in Minnesota and California (Figures 7, 8, and 9). In formerly species-rich heathlands across Western Europe, human-driven nitrogen deposition has been blamed for great losses of biodiversity in recent decades. In the Netherlands, high human population density, intensive livestock operations, and industries have combined to generate the highest rates of nitrogen deposition in the world. One well-documented consequence has been the conversion of species-rich heathlands to species-poor grasslands and forest. Not only the species richness of the heath but also the biological diversity of the landscape has been reduced because the modified plant communities now resemble the composition of communities occupying more fertile soils. The unique species assemblage adapted to sandy, nitrogen-poor soils is being 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 the nutrient ratios in tree leaves generally have been observed only in certain types of forests. These include high-elevation sites that receive large nitrogen deposits and sites with shallow soils containing few alkaline minerals to buffer acidification. Elsewhere in the U.S., the early stages of nitrogen saturation have been seen in response to elevated nitrogen deposition in the forests surrounding the Los Angeles Basin and in the Front Range of the Colorado Rockies. Some forests have a very high capacity to retain added nitrogen, particularly regrowing forests that have been subjected to intense or repeated harvesting, an activity that usually causes severe nitrogen losses. Overall, the ability of a forest to retain nitrogen depends on its potential for further growth and the extent of its current nitrogen stocks. Thus, the impacts of nitrogen deposition are tightly linked to other rapidly changing human-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 nitrogen are a fact of life in most natural ecosystems, and many native plant species are adapted to function best under 9 Figure 6-Deposition of nitrogen from the atmosphere is believed to be responsible for the yellowing and loss of needles from conifers and for cases of forest dieback, such as that shown here. Photo by John Aber Issues in Ecology Number 1 Spring 1997
Issues in Ecology Number Spring 1997 Losses of biodiversity driven by nitrogen deposi- Again not surprisingly,nitrate concentrations in tion can in tum affect other ecologica Re cent experiments in Minnesota grasslands showedth the world's la ong with the densi Amounts of tota in ecosystems made species-poor by fertilization.plant dissolved nitrogen in rivers are also correlated with hu productivity was much less stable in the face of a maior man population density,but total nitrogen does not in drought.Even in non-drought years,the normal vagar crease as rapidly as the nitrate fraction.Evidence indi ies of climate produced much more year-to-year varia- cates that with increasing human disturbance,a higher tion in the productivity of species-poor grassland plots than in more diverse plots. theiroactescom centration EFFECTS ON AQUATIC of nitrate have also been ob ECOSYSTEMS served in groundwater in many agricultural regions.al Historical Changes in Water though the magnitude of the Chemistru trend is difficult to deter ine in all but a few well-char trogen concentrations in sur terized aquifers. Overall.th face waters have increased as additions to groundwater human activities have acceler probably represent only a ated the rate of fixed nitrogen small fraction of the increased being put into circulation.A nitrate transported in surface recent study of the North At- waters.However.groundwa lantic Ocean Basin by scien ter hasan residence tim tistsfro a dozen nations es many aquifers,me timates that movements of to that groundwater quality is tal dissolved nitrogen into likely to continue to decline as most of the temperate-zone long as human activities are rivers in the basin may have having substantial impacts on increased by two-to 20-fold the nitrogen n cycle since Figure 7-Different rates of nitrogen addition lead to High levels of nitrates in marked changes in the plant and insect species com drink ing water raise signifi Sea region,the nitrogen in positions and speicies diversity of these plots of grass cant human health concems crease may have been six-to land vegetation in minnesota.each plot is 4m x 4m especially for infants.Mi 20-fold.The nitrogen in- (about 13 ft x 13 ft),and has received experimental crobes in an infant's stomach creases in these rivers are addition of nitrogen (ammonium nitrate)since 1982. may convert high levels of ni highly correlated with human trate to nitrite When nitrite ted inputs of nitr e ttheir watersheds.and is absorbed into the bloodstre onverts carryi g ctive deposition. -an anemi For decades.nitrate concentrations in many riv condition known as methemoglobinemia- can caus ers and drinking water supplies have been closely moni brain damage or death.The condition is rare in the U.S. tored in developed regions of the world,and analysis of but the potential exists whenever nitrate levels exceed these data confirms a historic rise in nitrogen levels in U.S.Public Health Service standards(1O milligrams per the nit ate ers In 1.000 lake in No liter). els doubled in less than Nitrogen and Acidification of Lakes since 1965.In major rivers of the northeastern U.S.. Nitric acid is playing an increasing role in the nitrate concentrations have risen three-to ten-fold since acidification of lakes and streams for two major reasons. the early 1900s,and the evidence suggests a similar One is that most efforts to control acid deposition- trend in many European rivers. which includes acid rain.snow.fog.mist.and dry depos
Losses of biodiversity driven by nitrogen deposition can in turn affect other ecological processes. Recent experiments in Minnesota grasslands showed that in ecosystems made species-poor by fertilization, plant productivity was much less stable in the face of a major drought. Even in non-drought years, the normal vagaries of climate produced much more year-to-year variation in the productivity of species-poor grassland plots than in more diverse plots. EFFECTS ON AQUATIC ECOSYSTEMS Historical Changes in Water Chemistry Not surprisingly, nitrogen concentrations in surface waters have increased as human activities have accelerated the rate of fixed nitrogen being put into circulation. A recent study of the North Atlantic Ocean Basin by scientists from a dozen nations estimates that movements of total dissolved nitrogen into most of the temperate-zone rivers in the basin may have increased by two- to 20-fold since preindustrial times (Figure 10). For rivers in the North Sea region, the nitrogen increase may have been six- to 20-fold. The nitrogen increases in these rivers are highly correlated with humangenerated inputs of nitrogen to their watersheds, and these inputs are dominated by fertilizers and atmospheric deposition. For decades, nitrate concentrations in many rivers and drinking water supplies have been closely monitored in developed regions of the world, and analysis of these data confirms a historic rise in nitrogen levels in the surface waters. In 1,000 lakes in Norway, for example, nitrate levels doubled in less than a decade. In the Mississippi River, nitrates have more than doubled since 1965. In major rivers of the northeastern U.S., nitrate concentrations have risen three- to ten-fold since the early 1900s, and the evidence suggests a similar trend in many European rivers. Again not surprisingly, nitrate concentrations in the worlds large rivers rise along with the density of human population in the watersheds. Amounts of total dissolved nitrogen in rivers are also correlated with human population density, but total nitrogen does not increase as rapidly as the nitrate fraction. Evidence indicates that with increasing human disturbance, a higher proportion of the nitrogen in surface waters is composed of nitrate. Increased concentrations of nitrate have also been observed in groundwater in many agricultural regions, although the magnitude of the trend is difficult to determine in all but a few well-characterized aquifers. Overall, the additions to groundwater probably represent only a small fraction of the increased nitrate transported in surface waters. However, groundwater has a long residence time in many aquifers, meaning that groundwater quality is likely to continue to decline as long as human activities are having substantial impacts on the nitrogen cycle. High levels of nitrates in drinking water raise significant human health concerns, especially for infants. Microbes in an infants stomach may convert high levels of nitrate to nitrite. When nitrite is absorbed into the bloodstream, it converts oxygencarrying hemoglobin into an ineffective form called methemoglobin. Elevated methemoglobin levels an anemic condition known as methemoglobinemia can cause brain damage or death. The condition is rare in the U.S., but the potential exists whenever nitrate levels exceed U.S. Public Health Service standards (10 milligrams per liter). Nitrogen and Acidification of Lakes Nitric 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- 10 Figure 7-Different rates of nitrogen addition lead to marked changes in the plant and insect species compositions and speicies diversity of these plots of grassland vegetation in Minnesota. Each plot is 4m x 4m (about 13 ft x 13 ft), and has received experimental addition of nitrogen (ammonium nitrate) since 1982. Photo by D. Tilman Issues in Ecology Number 1 Spring 1997