encyclopedia of inland waters || nitrogen

NitrogenR Howarth, Cornell University, Ithaca, NY, USA

ã 2009 Elsevier Inc. All rights reserved.

Introduction

Nitrogen is an essential element for life and is thefourth most abundant element in the living biomass(by moles) after hydrogen, carbon, and oxygen.Nitrogen is in all amino acids and nucleotides, andtherefore in all proteins and nucleic acids. Nitrogen isalso a major component of the chitin that makes upthe cell walls of fungi and the exoskeletons of aquaticinsects and crustaceans. Together with phosphorus,nitrogen limits rates of primary production in most ofthe ecosystems on Earth, including inland waters.However, unlike phosphorus, nitrogen has a veryactive oxidation–reduction cycle, and nitrogen innature exists in valence states from �3 to þ5. Curi-ously, and unlike the biogeochemical cycle of anyother major element, most of the nitrogen on Earthis present with an intermediate valence state of 0 (asmolecular N2). More than any other major elementcycle, human activity has accelerated the nitrogencycle leading to many critical changes in the aquaticecosystems.

Forms and Transformations of Nitrogen

Nitrogen occurs as both organic and inorganic nitro-gen in aquatic ecosystems. Frequently, the organicforms dominate, including both particulate organicnitrogen (PON) and dissolved organic nitrogen(DON). The PON not only includes the nitrogen inliving organisms, but also large amounts of nitrogenin detritus or dead organic matter. The DON consistsof a wide range of organic substances, including sim-ple substances such as free amino acids. Much of theDON, however, consists of higher molecular weightcompounds. Most of the DON in natural watershas never been chemically characterized because ofthe analytical challenge of measuring thousandsof unknown substances, each present at relativelylow concentrations.The inorganic nitrogen in aquatic ecosystems

includes dissolved N2 gas, oxidized ions such asnitrate (NO�

3 ) and nitrite (NO�2 ), the reduced ammo-

nium ion (NH4þ), and the reduced ammonia gas

(NH3). Nitrate is the most oxidized form of nitrogen(valence state ofþ5), while ammonia and ammoniumare most reduced (valence state of�3). Ammonium isa weak acid that is in equilibrium in a solution with

ammonia gas, which is a base. The equilibrium con-stant for this relationship is 10�9.3. Thus, ammoniumis more dominant whenever the pH is less than 9.3, asis generally true in aquatic ecosystems. At pH ¼ 8.3,the ammonium concentration is 10-fold greater thanthe ammonia concentration. At pH ¼ 7.3, the ammo-nium concentration is 100-fold greater than theammonia concentration. Since ammonia is a gas, itcan be volatilized to the atmosphere. The rate of lossis a function of the ammonia concentration, and sothis process is much greater at higher pHs, wherehigher concentrations of ammonia are favored.

Most of the nitrogen on the Earth is present as N2

gas. This becomes biologically available only throughbacterial nitrogen fixation, fixation by lightning orvolcanic activity, or fixation by human activity.Before the industrial revolution, bacterial nitrogenfixation was by far the major mechanism for thecreation of reactive, biologically available forms ofnitrogen on the planet. Increasingly, human activity isfixing nitrogen, and this dominates the nitrogen cyclein many regions, as discussed below.

The primary forms of reactive nitrogen assimila-ted by algae, rooted plants, fungi, and bacteriaare nitrate, nitrite, ammonium, and ammonia. Oncetaken up, nitrate and nitrite are reduced to ammo-nium in a process called assimilatory nitrate or nitritereduction. Ammonium – whether taken up directly orformed by assimilatory reduction in the organism – isused by plants, algae, and microorganisms to produceorganic nitrogen compounds. The organic nitrogen ofplants, algae, and microorganisms can flow through afood web to animals, and detrital PON and DON isdecomposed by bacteria and fungi. The organic nitro-gen eaten by animals or decomposed by microorgan-isms is excreted as ammonium or sometimes as urea,a low-molecular weight compound that is quicklyhydrolyzed to ammonium in water. These processesof releasing nitrogen back to the environment arecalled nitrogen mineralization (Figure 1).

The forms of inorganic, reactive nitrogen are con-verted from one to another in aquatic ecosystemsthrough a variety of bacterially mediated processes.Ammonium is oxidized to nitrate in a process callednitrification, an energy-yielding process. The nitrify-ing bacteria that catalyze the reaction gain energy anduse this energy to fix carbon dioxide into new bac-terial biomass, a process called chemosynthesis. Theenergy yield of the reaction is low compared with

57

58 Inorganic Chemicals _ Nitrogen

many chemosynthetic processes based on oxidizingsulfur or iron compounds, and so the growth of nitri-fying bacteria is slow. Nitrification rates are in part afunction of the population size of nitrifying bacteria;where mortality on the bacteria is high due to grazing,the slow growth result keeps population sizes low,and rates of nitrification can be very low, allowingammonium to accumulate.Nitrate is reduced to nitrite and nitrite is reduced to

N2 in a process called denitrification or dissimilatorynitrate reduction. The bacteria that catalyze thesereactions are heterotrophic bacteria that gain theirenergy from the degradation or organic matter; theyuse the nitrate or nitrite as an electron acceptor, verymuch as plants and animals and many other micro-organisms use oxygen as an electron acceptor forrespiration. Since the energy yield of respiring organic

Table 1 Summary characteristics of some key nitrogen-cycle proc

Nitrification: NH4þ þ O2 ! NO3

� þ H2O þ 2

Energy-releasing reaction; th

growth of chemo-autotoropTwo protons worth of acidity

process tends to make the

Denitrification: Organic matter þ NO3� þ Hþ

Energy releasing reaction, wi

bacteria that carry out this r

and gain approximately 90%

One proton of acidity is consuthe pH of the environment.

Nitrogen fixation (by photosynthetic

cyanobacteria):

1=2 N2 þ 3=2 H2O þ Hþ ! N

Nitrogen fixation requires an

photosynthesis, which cleavcost of the reaction is only p

environment, and can includ

assimilating necessary trac

One proton of acidity is consraise the pH of the environm

Nitrification

NH3

NO3–

N2

N2O, NO, NO2

Organic N inplants and algae

Organic N inanimals and microbes

Denitrification

Bacterial Nfixation

Figure 1 Simplified diagram of the nitrogen cycle in aquatic

ecosystems. Reprinted from Howarth (2002).

matter using nitrate as the electron acceptor is some-what less than when using oxygen as the electronacceptor, denitrification tends to occur only whenoxygen is absent or present at very low levels. Thiscondition is frequently the case in aquatic sediments,and often in the bottom waters of stratified lakes andestuaries. Denitrification is the major sink for reactivenitrogen in natural ecosystems. At the global scale,denitrification serves to balance nitrogen fixation andmaintains N2 gas as the major form of nitrogen on theplanet (Table 1).

Other nitrogen cycle processes have been discov-ered in the past few decades. One of these is denitrifi-cation based on chemosynthetic oxidation of sulfideor reduced iron rather than respiration of organicmatter. Another is the anaerobic oxidation of ammo-nium to N2 (ANAMOX), which is also a chemosyn-thetic process. And a third is the dissimilatoryreduction of nitrate to ammonium (DNRA). TheDNRA process is sometimes a form of respiration,with organic matter being consumed using nitrateas the electron acceptor; however, the nitrogen isreduced to ammonium rather than to N2. Dissimila-tory reduction of nitrate to ammonium can also occurthrough fermentation of organic matter or throughchemosynthesis associated with oxidation of sulfides.Unlike denitrification, DNRA conserves the nitrogenin the ecosystem in a reactive, biologically availableform. The relative importance of these newly discov-ered processes in natural ecosystems remains quiteuncertain. The amount of organic matter, the carbonto nitrogen ratio of the organic matter, and theamounts of sulfides and iron in sediments may allplay a role in determining which of these bacterialnitrogen-cycle processes is dominant (Figure 2).

esses

Hþ

e rather small quantity of energy released is used to support the

hic nitrifying bacteria that catalyze the reaction.are produced for every ammonium ion that is oxidized, so this

environment more acidic.

! 5=4 CO2 þ 1=2 N2 þ 5=4 H2Oth the energy coming from the respiration of organic matter; the

eaction use nitrate rather than oxygen as an electron acceptor,

of the energy yield compared to oxygen-based respiration.

med for every nitrate ion consumed, so this process tends to raise

H4þ þ 3=4 O2

input of energy; in this case, the energy is coming from

es oxygen to gain electrons and produces oxygen. Note that theart of the cost of nitrogen fixation. The total cost varies with the

e substantial costs for building and protecting enzymes and

e metals.

umed for every atom of nitrogen fixed, so this process tends toent.

High Fe

Low Fe

High C:N

Fe oxidation:denitrif to N2

Respirdenitrif to N2

FermentDNRA

Respirdenitrif to N2

Respirdenitrif to NO2

– thenanammox

S oxidizers:denitrif to N2

S oxidizersdomina to

S oxidizers:DNRA to NH4

+

High Cinputs

Low Cinputs

Not sulfidic

Sulfidic

High C:N

Low C:N

FeS, S�

H2S

Low C:N

Figure 2 Hypothesized controls on denitrification, DNRA, ANAMOX, and similar processes in aquatic sediments based on thelevel of organic matter inputs to the sediments, the amount of sulfides present, the amount of iron present, and the ratio of carbon to

nitrogen in the organic matter in the sediments. Reprinted from Burgin and Hamilton (2007).

Inorganic Chemicals _ Nitrogen 59

Nitrogen Cycling at the Ecosystem Scale

The nitrogen budget of most inland water ecosystemsis dominated by nitrogen inputs from upstream sys-tems, including inputs from streams and rivers and ingroundwaters. As discussed elsewhere within thisencyclopedia, bacterial nitrogen fixation can be animportant source, but in most aquatic ecosystemsthis is far less than the inputs from upstream sources.Direct deposition from the atmosphere can also be animportant input of nitrogen, that is nitrogen inputs inrain and snowfall as well as uptake of nitrogen gasesby the water body from the atmosphere and deposi-tion of nitrogen particles onto the water surface.However, only in aquatic ecosystems with verysmall watersheds does the direct deposition of nitro-gen from the atmosphere rival the input of nitrogen instream and river flow and in groundwaters.In most aquatic ecosystems, the rate of nitrogen

uptake by plants, algae, and microorganisms is fargreater than the rate of inputs from external sources,and the nitrogen needs of primary production anduptake by bacteria and fungi is supported by rapidrecycling of nitrogen within the ecosystem. In oligo-trophic lakes, the rate of uptake of nitrate and ammo-nium by phytoplankton is generally 50- to 100-foldmore than the rate of input of nitrogen from externalsources. In highly productive eutrophic lakes, the rateof nitrogen uptake by phytoplankton is often 10- to30-fold greater than the rate of external inputs. Insome very productive coastal salt marshes with huge

inputs of nitrogen delivered by twice-daily tides,nitrogen uptake by the primary producing organismsis roughly equal to the external nitrogen inputs, butthis is an extreme case of very high inputs.

In streams and rivers, the uptake of nitrogen andother nutrients can be considered in the context ofspiraling distances, or the average distance overwhich an atom flows before being assimilated byplants, algae, bacteria, or fungi. In streams that arenot heavily impacted by humans, this distance may bejust meters to perhaps a hundred meters. After assim-ilation, the nitrogen atom is eventually remineralizedand moves downstream again; again, on average, itmoves the same spiraling distance. In larger rivers, thedistances can be much greater, up to tens or hundredsof kilometers or even greater. And in landscapes withheavy human influences, the distances can be muchgreater; for instance, the spiraling distance for nitro-gen in a ditch draining agricultural lands may bekilometers or more.

Denitrification can be a major sink of nitrogenin aquatic ecosystems, including wetlands, lakes,reservoirs, estuaries, streams, and rivers. In lakes, reser-voirs and estuaries, rates of denitrification can be veryhigh when the water column is anoxic, as frequentlyoccurring in the bottom waters of stratified systems.Rates can also be high in the sediments of virtually allinland water ecosystems due to low oxygen levels.Commonly in many sediments and in wetland soils,nitrification and denitrification co-occur in close


proximity in microzones where oxygen is present (fornitrification) and absent (for denitrification). Thiscoupled nitrification–denitrification can account fora majority of the denitrification in aquatic ecosys-tems. The coupling of these processes is favored bythe bio-irrigating activities of animals and by therhizosphere of vascular plants.In aquatic ecosystems with an oxygenated water

column, the percentage of the nitrogen inputs thatare denitrified is well predicted as a function of thewater residence time and the depth of the water. Thisreflects the interaction time of the nitrogen with thesediments, the site of denitrification. The percentageloss of nitrogen is greater in ecosystems that are shal-lower and that have longer water residence times. Atthe landscape scale, the water residence time is fre-quently more important. Thus, the loss of nitrogenthrough denitrification tends to be greater in lakesand reservoirs than in streams and rivers (Figure 3).

Nutrient Limitation of Net PrimaryProduction

Relative to the need for other essential elements byrooted plants and algae, nitrogen is frequently inshort supply. As a result, nitrogen limits rates of netprimary production in many types of both aquaticand terrestrial ecosystems. Either nitrogen or phos-phorus limits primary production in almost all eco-systems on Earth, except for some 10% of the area ofthe world’s oceans where iron may be limiting. Forinland waters, both nitrogen and phosphorus areoften important limiting factors, and some interestingpatterns of nutrient limitation occur across differenttypes of inland waters. For instance, in the TemperateZone in ecosystems of moderate to high productivity,phosphorus is more generally limiting in freshwater

Lakes and reservoirs

River stretches

00

50

100

100 200 300

%

Mean depth/residence time (myr–1)

Figure 3 The percentage of nitrogen inputs to aquaticecosystems that is lost through denitrification as a function of

depth and residence time of the system. Modified from Howarth

et al. (1996).

lakes and nitrogen in estuaries. This has importantramifications for the management of eutrophication(excess production) in these ecosystems. As is dis-cussed in the section below, human activity hasgreatly accelerated the nitrogen cycle, leading to mas-sive increases in nitrogen inputs to estuaries in manyparts of the world. Nitrogen is now the largest sourceof pollution in estuaries, and in the United States,two-thirds of estuaries are moderately to severelydegraded from nitrogen pollution and the eutrophi-cation it causes.

Whether nitrogen or phosphorus is more limiting isa function of the relative availabilities of these twoelements in the ecosystem. Although there is someplasticity in the elemental composition of phyto-plankton, the variation is surprisingly small and theratio of nitrogen to phosphorus in phytoplanktonbiomass is usually in the range of 16:1 by moles (the‘Redfield ratio’, named after Alfred Redfield whodescribed the relationship between water chemistryand phytoplankton composition in the world’s oceansin the 1930s). In ecosystems where the ratio of avail-able nitrogen to phosphorus in the water is well above16:1, phosphorus is in relatively short supply and willbe more limiting to net primary production. In eco-systems where the nitrogen:phosphorus ratio of avail-able nutrients is well below 16:1, nitrogen is inrelatively short supply (compared with the needs ofthe phytoplankton) and will be more limiting. Theratio of dissolved inorganic nitrogen (the sum ofnitrate, nitrite, ammonium, and ammonia) to dis-solved inorganic phosphorus is a reasonable indicatorof the ratio of dissolved nitrogen and phosphorus inmany cases and can be used to infer whether nitrogenor phosphorus is more limiting, if the ratio is suffi-ciently above or below 16:1. However, dissolved inor-ganic nutrients often recycle quite quickly in thewater column of aquatic ecosystems, and so concen-trations are not always a reliable indicator of supply.Further, most analytical methods for measuring dis-solved inorganic phosphorus overestimate this quan-tity by some unknown amount due to inclusion ofsome organic phosphorus and positive interferencefrom arsenic.

The ratio of available nitrogen to phosphoruswithin an ecosystem is a function of both the ratioin the external inputs of these elements and the pro-cessing of nitrogen and phosphorus within the eco-system. Often, the nitrogen to phosphorus ratio innutrient inputs from watersheds are well above16:1, which tends to drive the aquatic ecosystemstowards phosphorus limitation. In contrast to lakes,estuaries receive nutrients both from upstream water-sheds and from ocean waters. The ocean waters arefrequently phosphorus rich and somewhat depleted in


nitrogen (relative to the Redfield ratio). This is one ofthe reasons that estuaries are more prone to nitrogenlimitation.A variety of processes within an ecosystem can

change the availabilities of nitrogen and phosphorus.Of particular importance for phosphorus is theadsorption to sediment particles. This lowers concen-trations of dissolved inorganic phosphorus, andtherefore makes phosphorus limitation more likely.The presence of competing ions in seawater makesadsorption less in estuaries than in freshwaters, andinorganic phosphorus that is adsorbed to suspendedsediment particles in rivers is largely desorbed andbecomes soluble in estuaries as the salinity increases.This tends to make phosphorus limitation less likely(and nitrogen limitation more likely) in estuaries thanin freshwater ecosystems (within the constraints setby the inputs of nitrogen and phosphorus, and theinfluences of other biogeochemical processes).Both nitrogen fixation and denitrification can have

large influences on the availability of nitrogen inaquatic ecosystems. Nitrogen fixation is discussed indetail elsewhere within this encyclopedia. Briefly,nitrogen fixation by planktonic cyanobacteria is animportant process in many lakes that helps to allevi-ate nitrogen shortages and contributes to phosphoruslimitation in freshwaters. In stark contrast, nitrogenfixation by planktonic cyanobacteria seldom, if ever,occurs in even strongly nitrogen-limited estuaries atsalinities greater than 10 parts per thousand. This isprobably a result of the high sulfate concentrations inseawater interfering with the uptake of molybdenumby planktonic cyanobacteria in estuaries; molybde-num is required for nitrogen fixation. It is interestingto note that sulfate levels are sometimes high andsometimes not in inland saline lakes. As a result,nitrogen fixation is a major process in some salinelakes but not in others. In saline lakes where nitrogenfixation occurs, the process helps to alleviate nitrogenshortages and maintain phosphorus limitation, whilehigh sulfate lakes without significant nitrogen fixa-tion are often nitrogen limited.We have an imperfect understanding of whether

nitrogen or phosphorus is more limiting in manytypes of aquatic ecosystems, including oligotrophic(low-productivity) lakes andmany tropical reservoirs,particularly for those systems where the ratio of dis-solved inorganic nitrogen to phosphorus is too close tothe Redfield ratio of 16:1 to allow for unambiguousinterpretation. Often, researchers will use short-termbioassays to evaluate nutrient limitation. In thisapproach, nitrogen, phosphorus, or some other ele-ment is added to water samples in bottles and anychange in phytoplankton biomass or productivityover a few days to a week is noted. While this can

provide very useful information, the approach hasmany difficulties. One of the greatest difficulties isthat the time frame may not allow for some importantbiogeochemical processes, such as nitrogen fixation,to occur. In experiments with nutrient additions towhole lakes over growing seasons and years, research-ers have demonstrated that temporary shortages ofnitrogen that result from fertilizing with phosphorusand nitrogen at ratios below 16:1 can be alleviated byplanktonic nitrogen fixation, and that the lakesremain phosphorus limited over these longer timeframes. But such a response would not be observedin a short-term bioassay, which might instead suggestnitrogen limitation. The nitrogen limitation would infact be only a short, transient feature.

The most robust information on nutrient limitationin aquatic ecosystems has come from longer-term,whole-ecosystem experiments and experiments withlarge tanks or bags designed to mimic important com-ponents of the ecosystem over time periods of a grow-ing season or longer (mesocosm experiments). Suchexperiments have clearly shown a prevalence forphosphorus limitation in moderately productivelakes and for nitrogen limitation in estuaries in theTemperate Zone. The lack of such experiments intropical systems and in low-productivity temperatesystems to date constrains our understanding of nutri-ent limitation.

Human Acceleration of the Nitrogen Cycle

Human activity has altered the nitrogen cycle morethan that of any other major element on Earth. Priorto the industrial and agricultural revolutions, thevast majority of reactive nitrogen on the planet wascreated by bacterial nitrogen fixation, and this rateof creation was balanced over geological time bydenitrification. Now the creation of nitrogen byhumans to produce synthetic nitrogen fertilizerthrough the Haber–Bosch process rivals the rate ofnatural fixation on the continents. The inadvertentcreation of reactive nitrogen during fossil fuel com-bustion also adds to the global nitrogen cycle.

The influences of human activity on the nitrogencycle vary across the regions of the globe. Because ofthe high chemical reactivity and high biologicaldemand for nitrogen, most forms of reactive nitrogen(i.e., nitrogen other than N2 gas) do not cycle glob-ally, but rather at the scale of large regions. Thenatural rates of nitrogen fixation in terrestrial ecosys-tems are much higher in the tropics, whereas most ofthe fertilizer use and fossil fuel combustion to datehas occurred in temperate regions. This is changingsomewhat as fertilizer use and fossil fuel combustion


increase in South Asia and tropical South America.Nonetheless, to date the largest changes in nitrogencycling have occurred in the developed countries inthe Temperate Zone. The flow of nitrogen in largerivers in these areas has increased 15-fold or more dueto human activity, with much of this increase occur-ring in the past three to four decades (Figure 4).Globally, the use of synthetic nitrogen fertilizer

has driven most of the increase in nitrogen cycling.However, in some regions such as the northeasternUnited States, the combustion of fossil fuel has beena larger contributor. This fossil fuel combustion leadsto pollution of the atmosphere with oxidized nitrogencompounds. Their deposition onto the landscape con-tributes to the flux of nitrogen to aquatic ecosystems.Much of the nitrogen is deposited onto forests, whichretain a great deal of it, and some falls on urban andsuburban lands, where retention is much less.The largest consequence on aquatic ecosystems

of the human acceleration of the nitrogen cycle hasbeen the eutrophication of estuaries and other coastalwaters. The resulting eutrophication has led tooxygen-deprived waters (anoxic and hypoxic zones,sometimes called ‘dead zones’) in many areas, as wellas habitat degradation, loss of biotic diversity, andincreased incidences and extent of harmful algalblooms. In the Temperate Zone, nitrogen has prob-ably not led to eutrophication in many freshwaterecosystems simply because phosphorus limitation isso muchmore prevalent. However, increased nitrogeninputs to some tropical lakes such as Lake Victoria inAfrica may well be contributing to eutrophication.A larger impact of accelerated nitrogen cycling on

freshwater ecosystems in the Temperate Zone comes

Natural background flux

Republic of Korea

North Sea watersheds

Northeastern U.S.

Yellow River basinMississippi River basin

Baltic Sea watershedsSt. Lawrence River basin

Southwestern Europe

Labrador and Hudson’s Bay

0 500 1000 1500 2000

Figure 4 The flux of nitrogen in rivers expressed per area of

watershed for contrasting areas in the Temperate Zone. Units

are kg N km�2 yr�1. The natural background flux in Temperate

Zone regions without human disturbances is estimated to beroughly 100 kg N km�2 yr�1. Based on information in Howarth

et al. (2005).

from acid rain. Both sulfuric and nitric acids contrib-ute to acid rain. Much of the focus historically hasbeen on sulfuric acid, and that has led to some mea-surable progress in reducing sulfur emissions to theatmosphere. Reductions in NOx, the precursor fornitric acid, have been far less, and nitric acid is there-fore growing as an overall source of acid rain. Thisnitric acid – which comes from fossil fuel combustionand is the same nitrogen deposition that contributesto nitrogen flows to estuaries – is the major source ofacid rain now in some regions.

The deposition of ammonia gas and ammoniumparticles can also contribute to the acidification ofinland waters. Most of the ammonia in the atmos-phere comes from volatilization from agriculturalsources, and particularly from large animal feedlotoperations. Ammonia is a base, and so acts to raisethe pH of precipitation. In this technical sense,ammonia counteracts acid rain. However, the ammo-nia and ammonium deposited onto terrestrial ecosys-tems or directly onto aquatic ecosystems can benitrified to nitrate, as discussed above. This chemicaltransformation produces large quantities of acid – 1mole of proton acidity generated for every mole ofnitrate created. Consequently, the deposition ofammonia and ammonium also can contribute sub-stantially to the acidification of inland waters.

Nitrate in drinking water for humans is also ofconcern, and a standard of 10 mg nitrate-N per literis set in most of the world’s nations, based on advicefrom the World Health Organization. Such a stan-dard has existed for many decades in the UnitedStates, and was originally set over concern about‘blue-baby syndrome,’ a disease in infants wherenitrate binds to hemoglobin in the blood, interferingwith oxygen transport, and turning the blood blue.Studies over the past few decades have suggested thatnitrate in drinking water poses other health risks,including risk of a variety of cancers and a variety ofdevelopmental issues, and perhaps at levels below thedrinking water standard. This topic has seen muchdebate in the past decade, with some arguing thatnitrate is a natural occurrence in saliva that thehuman body may actually manipulate to reduce bac-terial infection. However, evidence shows a strongcarcinogenic risk from nitrate in drinking water, prob-ably due to the formation of nitrosomines, which arehighly carcinogenic compounds. The best current evi-dence suggests a strong interaction between nitrateexposure and other dietary considerations: nitrate invegetables such as spinach seems to pose little risk,while nitrate in drinking water combined with ahigh red-meat and low vegetable and fruit diet posesa major risk. Nitrate in drinking water at levels


well below the current drinking water standard canpose a risk, in association with poor diet. Unfortu-nately, many of the drinking water sources in theworld – including the developed world – exceed thecurrent drinking water standard, and concentrationsof nitrate in drinking water are rising.Nitrogen poses health risks beyond those of direct

toxicity or carcinogenicity from nitrate, to bothhumans and natural animal populations. The toxicityof ammonia to aquatic animals is well known and is amajor problem in waters heavily polluted from sew-age or animal wastes. A more subtle aspect is theindirect effect of nitrogen on animal vectors thatcarry disease. Recent work has shown that parasiticdiseases of amphibians can increase markedly aseutrophication proceeds: nutrient pollution (proba-bly phosphorus) in freshwaters in Temperate-Zoneareas can lead to increased parasite releases fromsnails, which are an intermediary host, and causemassive disease in frogs and salamanders. Thedisease-causing organism is closely related to schisto-somiasis, a major disease for humans in many tropicalareas. An increase in snail populations as a result ofnitrogen-based eutrophication in tropical reservoirsand lakes could lead to a similarly large increasein schisotomiasis. The Temperate-Zone studies onamphibian disease show an increased risk of diseaseresulting not only from an increase in snail popula-tions as eutrophication progresses, but also a hugeincrease in the release of parasites from each snail.In another study, malaria has increased in somecoastal areas of Brazil due to nitrogen-inducedincreases in eutrophication in mangrove swampsleading to increased abundances of mosquitoes thatcarry the malaria parasite.One aspect of the human acceleration of the nitro-

gen cycle demands particular attention: the gasnitrous oxide (N2O) presents severe challenges tothe global environment. Laughing gas, as it issometimes called, is an effective pain-killing drugsometimes used by dentists. It is also a long-livedgas in the Earth’s atmosphere, with a residence timeestimated at 120 years. Concentrations are rising rap-idly. The gas catalyzes the destruction of ozone inthe stratosphere, and increasingly nitrous oxide isresponsible for ozone holes that allow excessiveUV-B radiation to penetrate to the Earth’s surface.Nitrous oxide is also a major absorber of infra-redenergy, and therefore is a potent greenhouse gasthat contributes to global warming. The Intergovern-mental Panel on Climate Change considers nitrousoxide to be nearly 300-fold more powerful thancarbon dioxide in terms of its long-term effect onglobal warming. Nitrous oxide is produced as a

leakage-produce of both nitrification and denitrifica-tion. The rapid increase in the concentration of thisgas in the atmosphere is clearly a side effect of theglobal acceleration of the nitrogen cycle by humanactivity.

Glossary

Anoxic – Oxygen-free, lacking oxygen.

Denitrification – The process of converting nitrateto molecular N2; also called dissimilatory nitratereduction.

Eutrophic – Characterized by high levels of primaryproduction and high algal biomass.

Hypoxic – Having oxygen present at only low con-centrations (generally less than 2 mg/l).

Nitrification – The oxidation of ammonium to nitriteand nitrate by bacteria.

Nitrogen fixation – The conversion of molecularN2 into reactive nitrogen compounds such asammonium.

Nutrient limitation – The condition of rate of growthof production by photo-autotrophs being less thanmaximum due to a constraint by one or more nutri-ents, usually phosphorus or nitrogen.

Oligotrophic – Characterized by low levels of pri-mary production and low algal biomass.

Oxic – Having oxygen present.

Primary production – The rate of accumulation ofnew biomass by plants, algae, and photosyntheticbacteria through photosynthesis.

Rhizosphere – The roots, rhizomes, and associatedmicro-organism of a vascular plant.

See also: Acidification; Alkalinity; Limnology as a Disci-pline; Micronutrient Elements (Co, Mo, Mn, Zn, Cu);Nitrogen Fixation; Phosphorus; Salinity.

Further Reading

Burgin AJ and Hamilton SK (2007) Have we overemphasized the

role of denitrification in aquatic ecosystems? A review of nitrate

removal pathways. Frontiers in Ecology & Environment 5:89–96.

Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN,

and Smith VH (1998) Nonpoint pollution of surface waters with

phosphorus and nitrogen. Issues in Ecology 3: 1–12.Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RH,

Cowling EB, and Cosby BJ (2003) The nitrogen cascade. BioSci-ence 53: 341–356.

Howarth RW (2002) The nitrogen cycle. In: Mooney HA andCanadell JG (eds.) Encyclopedia of Global EnvironmentalChange. The Earth System: Biological and Ecological


Dimensions of Global Environmental Change, Vol. 2,

pp. 429–435. Chichester: Wiley.Howarth RWand Marino R (2006) Nitrogen as the limiting nutri-

ent for eutrophication in coastal marine ecosystems: Evolving

views over 3 decades. Limnology and Oceanography 51:

364–376.Howarth RW, Billen G, Swaney D, Townsend A, Jarworski N,

Lajtha K, Downing JA, Elmgren R, Caraco N, Jordan T,

Berendse F, Freney J, Kueyarov V, Murdoch P, and Zhao-liang

Zhu (1996) Riverine inputs of nitrogen to the North AtlanticOcean: Fluxes and human influences. Biogeochemistry 35:

75–139.

Howarth RW, Ramakrishna K, Choi E, Elmgren R, Martinelli L,

Mendoza A, Moomaw W, Palm C, Boy R, Scholes M, andZhao-Liang Zhu (2005) Chapter 9: Nutrient Management,

Responses Assessment. In: Ecosystems and Human Well-being,

Policy Responses, the Millennium Ecosystem Assessment,Vol. 3,pp. 295–311. Washington, DC: Island Press.

Seitzinger SP, Styles RV, Boyer EW, Alexander R, Billen G, Howarth

R, Mayer B, and van Breemen N (2002) Nitrogen retention in

rivers: model development and application to watersheds in the

northeastern US. Biogeochemistry 57&58: 199–237.Townsend AR, Howarth R, Bazzaz FA, Booth MS, Cleveland CC,

Collinge SK, Dobson AP, Epstein PR, A Holland E, Keeney DR,

Mallin MA, Rogers CA, Wayne P, and Wolfe AH (2003) Human

health effects of a changing global nitrogen cycle. Frontiers inEcology & Environment 1: 240–246.

Vitousek PM, Aber J, Bayley SE, Howarth RW, Likens GE, Matson

PA, Schindler DW, Schlesinger WH, and Tilman GD (1997)

Human alteration of the global nitrogen cycle: Causes and con-sequences. Ecological Applications 7: 737–750.

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