Gayana Bot. 62(2): 98-109, 2005 ISSN 0016-5301

ARTÍCULOS REGULARES

ALTERATION OF NITROGEN CYCLING BY AGRICULTURAL ACTIVITIES, AND ITS ENVIRONMENTAL AND HEALTH CONSEQUENCES

ALTERACION DEL CICLO DEL NITROGENO POR LAS ACTIVIDADES AGRICOLAS, SUS CONSECUENCIAS AMBIENTALES Y SOBRE LA SALUD HUMANA

Oswald van Cleemput & Pascal Boeckx

Laboratory of Applied Physical Chemistry - ISOFYS, Faculty of Biosciences Engineering, Ghent University, Coupure 653, 9000 Gent, Belgium. oswald.vancleemput@ugent.be

ABSTRACT

The food demands of the increasing world population puts pressure on land use and N availability. In this paper an overview is given of the different N cycling processes affected by agricultural activities. Of the amount of N added to the soil, about half is removed from the field as harvested crop, while the remainder of the N is incorporated into soil organic matter or is lost to other parts of the environment. During the last decades there has been much research on environmental consequences of agricultural activities, mainly on emission of gaseous N compounds (NH₃, NO, N₂O and N₂), but also on N leaching, runoff and erosion. Study of the factors controlling loss of N is complex because of their multiplicity and mutual interactions. More recently attention is also going to human health problems as a consequence of agriculture. Nitrate in food and drinking water, ozone depletion in the stratosphere, ozone formation in the troposphere, global warming and its consequences, acidification and eutrophication are among the phenomena influencing life on Earth.

Keywords: Acidification, drinking water, eutrophication, greenhouse effect, nitrogen loss, ozone.

RESUMEN

La necesidad de alimentos para la creciente población humana significa una presión sobre el uso del suelo y la disponibilidad de nitrógeno. En este trabajo se entrega un resumen acerca de los diferentes procesos del ciclo del N que son afectados por las actividades agrícolas. De la cantidad total de N agregado al suelo, cerca de la mitad es removido desde el campo en la cosecha, mientras que el remanente de N es incorporado en la materia orgánica del suelo o perdido hacia otros compartimientos ambientales. Durante las últimas décadas una enorme cantidad de investigación se ha desarrollado acerca de las consecuencias ambientales de las actividades agrícolas, principalmente sobre la emisión de compuestos gaseosos de N (NH₃, NO, N₂O y N₂), y además sobre el lavado de N, escorrentía y erosión. El estudio de los factores que controlan las pérdidas de N es complejo debido a su multiplicidad e interacciones mutuas. Recientemente una mayor atención se está enfocando hacia los problemas en la salud humana como una consecuencia de la agricultura. Algunos de los problemas ambientales que influyen en la vida sobre la Tierra son, entre otros, el nitrato en los alimentos y en el agua potable, la disminución del ozono estratosférico, la formación del ozono en la tropósfera, el calentamiento global y sus consecuencias, la acidificación y la eutroficación.

Palabras claves: Acidificación, agua potable, efecto invernadero, eutroficación, ozono, pérdida de nitrógeno.

INTRODUCTION

The world population is expected to reach 8,000 million by 2020 and most increase will occur in the developing world (Lal 2000, Cakmak 2002). This population increase is causing pressures for increased food production resulting in worldwide land degradation and expansion of agriculture into marginal areas (Scherr 1999). Nevertheless, global food production has been tripled over the past 50 years (Mosier et al. 2004). Taking into account the limitations for bringing additional land into crop production, the yield per unit land will have to increase worldwide in the coming decades.

Among the mineral elements, N is taken up by plants in comparatively larger amounts than other nutrients and is usually responsible for yield increases of cultivated plants. Legumes and certain other plants in association with micro-organisms can obtain their N from the atmosphere, but most plants take their N from the soil. An increased use of N fertilizers at low level (as in most developing countries) will have beneficial effects on health (more and better food production), while an increased use at high level (as in most developed countries) might have more severe environmental risks. Fertilizer supplies about 50% of the total N required for global food production (Smil 1999). Worldwide, of the 170 Tg N added to the soil, about half is removed from the field in harvested crops, while the remainder is incorporated into soil organic matter or is lost to other parts of the environment. Global estimates of these loss processes are still highly uncertain.

Too little or too much N fertilizer can respectively influence human health or create environmental problems. Too often, analyses of crop productivity in general and soil N fertility problems in particular overlook interactions between food production and environmental impact, with consequences for human health. This paper tries to combine these aspects by covering the relevant aspects of the N cycle, N-related problems in the environment and the consequences for human health.

NITROGEN CYCLING AND AGRICULTURE

AGRICULTURAL ACTIVITIES AND NITROGEN TRANSFORMATIONS

The N cycle (Fig. 1) in terrestrial (and aquatic) ecosystems provides some understanding of the link between soil and fertilizer N, yield and environmental consequences. Starting with atmospheric N₂ gas (valency 0), lightning can convert it to various oxides and finally to nitrate (NO₃^-) (valency +5), which can be deposited and taken up by growing plants. Also N₂ gas can be converted to ammonia (NH₃, valency -3) by microbial fixation, with the NH₃ participating in a number of biochemical reactions in the plant. When plant residues decompose, the N-compounds will undergo a series of microbial conversions leading first to the formation of ammonium (NH₄⁺) (valency -3) and possibly ending up in NO₃^- (nitrification). Under anaerobic conditions, NO₃^- can be converted to various N-oxides and finally to N₂ gas (denitrification). When mineral or organic N fertilizers are used they also undergo the same transformation processes.

FIGURE 1. A simplified soil N cycle (top part is the areal zone, light grey the rooting zone, dark grey the subsoil) (Hofman & Van Cleemput 2004). FIGURA 1. Un N ciclo simplificado (parte más arriba es la zona areal, gris claro es la zona de raíces, gris oscuro es el subsuelo) (Hofman & Van Cleemput, 2004).

In considering the mineral N pool in the plant rooting zone, there can be N gains (such as microbial N-fixation) as well as N losses (such as leaching and denitrification). Furthermore, N can be exported from the soil via harvested products, or immobilized in soil organic matter (Fig. 2). Nitrogen is ubiquitously present, in aquatic as well as terrestrial environments.

FIGURE 2. Factors influencing the mineral N pool (Hofman & Van Cleemput 2004). FIGURA 2. Factores afectando el mineral N pool (Hofman & Van Cleemput, 2004).

The principal forms of N in the soil are NH₄⁺, NO₃^- and organic N-substances. At any moment, the inorganic N in the soil is only a small fraction of the total soil N. Growing plants get their N from fertilizer N as well as from organic soil N upon mineralization. A critical point is knowing the correct fertilization requirement, taking into account that the fertilizer is taken up in variable amounts. Application of fertilizers might also importantly influence the availability of native soil nutrients. A series of reactions occurs in the soil and determines the available N (Fig. 3). Especially N, but also other nutrients can participate in a series of reactions such as adsorption/desorption, mineralization/immobilization (MIT), nitrification, denitrification, as well as volatilization and leaching. It is important to realize that a number of reactions are in competition with each other and that some reactions lead to loss of nutrients from the system. The parameters influencing these loss reactions should be controlled to lower the risk of further degradation of water and air quality. The critical point is to make sure that plant nutrient uptake is the dominant process and that the other competing reactions do not become important. In other words, it is necessary that the efficiency of the fertilizer be as high as possible, while also optimizing all other nutritional conditions.

FIGURE 3. Competitive reactions for plant nutrients. FIGURA 3. Reacciones competitivas para nutrientes vegetales.

Microorganisms can use both NH₄⁺ and NO₃^- to satisfy their need for N. However, NH₄⁺ is preferred above NO₃^-. This type of N transformation is called microbial immobilization. The ratio between carbon (C) and N (C:N ratio) in organic matter determines whether immobilization or mineralization is likely to occur. When utilizing organic matter with a low N content, the microorganisms need additional N, decreasing the mineral N pool of the soil. Thus, incorporation of organic matter with a high C:N ratio (e.g. cereal straw) results in immobilization. Incorporation of organic matter with a low C:N ratio (e.g. vegetable or legume residues) results in N-mineralization. A value of the C:N ratio of 25 to 30 is often taken as critical point towards either immobilization or mineralization (Hofman & Van Cleemput 2004).

There should be a continuous concern to minimize losses of N into the atmospheric, terrestrial and aquatic environment. Indeed, N can easily be lost from the site of application in farmers' fields through soil erosion, runoff or leaching of nitrate or dissolved forms of organic N (Goulding 2004), or through gaseous emissions to the atmosphere as ammonia (NH₃), nitric oxides (NO and NO₂), nitrous oxide (N₂O), or dinitrogen (N₂) (Peoples et al. 1995). All these loss processes, with the exception of N₂, can potentially impact on one or more environmental hazards, and/or have important implications for human health.

NITROGEN LOSS PROCESSES

Ammonia volatilization

Losses of N from the soil by NH₃ volatilization amount globally to 54 Mt yr^-1 and 75% is of anthropogenic origin (Sutton et al. 1998). Galloway et al. (1995) estimated that of the 47 million ton of NH₃-N produced globally each year as a result of human activity, 32 Mt was associated with domestic animals, and 10 Mt volatilized from fertilized fields. According to ECETOC (1994) the dominant source is animal manure and about 30% of N in urine and dung is lost as NH₃. The other major source is surface application of urea or ammonium bicarbonate and to a lesser degree other ammonium-containing fertilizers. As urea is the most important N fertilizer in the world, it may lead to important NH₃ loss upon hydrolysis and subsequent pH rise in the vicinity of the urea prill. The transformation of NH₄⁺ to the volatile form NH₃ increases with increasing pH, temperature, soil porosity, and wind speed at the soil surface. It decreases with increasing water content and rainfall events following application. In general, ammonia has a short lifetime and can be deposited shortly after emission. This leads to acidification of the soil upon nitrification, depending on the buffer capacity of the soil.

EMISSION OF NITROGEN OXIDES (N₂O, NO) AND MOLECULAR NITROGEN (NITRIFICATION AND DENITRIFICATION)

Microbial nitrification and denitrification are responsible for the emission of nitrogen monoxide (NO) and nitrous oxide (N₂O) (Bremner 1997). They are byproducts in nitrification and intermediates during denitrification. Probably about 0.5% of fertilizer N applied is emitted as NO (Veldkamp & Keller 1997) and 1.25% as N₂O (Mosier et al. 1998). Intensification of arable agriculture and of animal husbandry has made more N available in the soil N cycle increasing the emission of N oxides. The relative percentage of NO and N₂O formation very much depends on the moisture content of the soil. At water-filled pore spaces (Fig. 4) below 60% the importance of nitrification increases with formation of NO. Between 60 and 80% denitrification becomes more important with formation of N₂O. From 75% on, the formation of N₂ by denitrification is dominant (Linn & Doran 1984, Davidson 1991). Next to the water content, also temperature and availability of N and decomposable organic matter are important determining factors for N₂O formation. Nitrous oxide is a greenhouse gas causing 5-6% of the enhanced greenhouse effect. Mosier (2001) reported that waste management of livestock excreta, direct emissions from cropping soils, and indirect emissions from N after it is leached or eroded from the site of application; each contributes equally to the 6.5 million ton of N₂O-N estimated to be derived annually from agriculture.

FIGURE 4. Influence of water-filled pore space on aerobic/anaerobic N transformation processes (Linn & Doran 1984). FIGURA 4. Influencia de "espacio de poros llenada de agua" sobre N transformaciones aerobos/anaerobos (Linn & Doran, 1984).

Nitrous oxide is a potent greenhouse gas, with a long half-life in the atmosphere (110-150 years, Peoples et al. 1995). Increased concentrations are also detrimental for the stratospheric ozone layer (Crutzen 1976). In the presence of sunlight, NO_x (NO and NO₂) react with volatile organic compounds from evaporated petrol and solvents and from vegetation and forms tropospheric ozone which is, even at low concentration, harmful to plants and human beings. The major gaseous end-product of denitrification is N₂. The ratio of N₂O to N₂ produced by denitrification depends on many environmental conditions. Generally, the more anaerobic the environment the greater the N₂ production is. Denitrification is primarily controlled by three factors (oxygen, nitrate and carbon) being controlled by several physical and biological factors. Denitrification N loss can reach 10% of the fertilizer N input; more on grassland and when manure is also applied (Von Rheinbaben 1990). Chemical denitrification is normally insignificant and is mainly related to the stability of NO₂^- and acid conditions (Van Cleemput 1998).

LEACHING, RUNOFF AND EROSION

Applied NO₃^- or NO₃^- formed through nitrification from mineralized NH₄⁺ or from NH₄⁺ from animal manure can leach out of the rooting zone. It is well possible that this leached NO₃^- can be denitrified at other places and return into the atmosphere. The amount and intensity of precipitation, quantity and frequency of irrigation, evaporation rate, temperature, soil texture and structure, land use managements, cropping and tillage practices and the amount and form of fertilizer N are all parameters influencing the amount of NO₃^- leaching to the underground water. Nitrate leaching should be kept under control as it may influence the nitrate content in drinking water influencing human health and in surface water, causing eutrophication. In hilly regions an important amount of topsoil can be displaced through runoff and erosion, carrying different amounts of N from one place to another.

FACTORS CONTROLLING PATHWAYS OF N LOSS

Table I provides a simplified summary of the important factors involved and indicates the complexity of N loss processes (Peoples et al. 2004). The controlling factors are divided into environmental variables, which are largely uncontrollable, and the impacts of human activity through which we have some ability to manage losses.

Each factor is ranked against each process according to its relative importance in controlling that process. The ranking includes both positive and negative effects. Each factor is considered entirely separately from each others. For example, in the field, water supply influences soil aeration, but Table I ignores such interactions. Topsoil texture is separated from soil profile because the former has a specific effect on biological processes, while the latter influences physical properties, e.g. hydrology. Available C is not just an environmental variable, but is also influenced by human activity. Although topography is a multi-determining factor, in Table I it is only considered as affecting slope. Nitrogen inputs include mineral fertilizer, manures, compost, biological N₂ fixation but not atmospheric deposition. Within tillage 'no till' does not include groundcover, and stocking rate is used as a more general term than grazing intensity. Human activity can influence almost every process listed in Table I, so control is possible but is likely to be complicated. The most important factors would appear to be N inputs, stocking rates of grazing animals, and land use change.

Denitrification is the most complex process and the one mostly influenced by environmental variables (Table I). One aspect of its complexity is the proportion of emissions as N₂O, which has important environmental consequences, or as N₂, which has no adverse implications (Peoples et al. 1995). The influence of different variables on the ratio of N₂O: N₂ in gaseous emissions is illustrated in Table II (Van Cleemput 1998).

The relative importance of the various loss processes will vary considerably across different regions based on climate, soils, dominant land use, and sources of N inputs used for agriculture (Goulding 2004). Estimates of the contributions of different countries or regions to the total global losses of N in a gaseous (e.g. IFA/FAO, 2001) or liquid phase (e.g. Van Drecht et al. 2003) are based on a wide range of assumptions and extrapolations from research findings and point source measurements. Clearly such derived estimates are likely to be more reliable for those regions and countries that are most 'data rich', and given the technical difficulties in measuring the different pathways of N losses, it is inevitable that more quantitative information at different levels of resolution will be available for some loss processes than others, and in some regions than others (Goulding 2004).

ENVIRONMENTAL AND HEALTH IMPACTS OF AGRICULTURAL ACTIVITIES

First, it is important to realize that in addition to the issues listed in this paragraph, there may be other less apparent environmental implications associated with the use of fertilizer compared to alternative sources of N. It appears that the additional global warming potential generated by the use of fossil energy to produce N fertilizers should also be considered when undertaking a full inventory of environmental consequences (Crews & Peoples 2004).

The input of reactive N into the soil has a wide range of impact on humans and ecosystems in different ways in various parts of the world (Galloway & Cowling 2002). Some of these changes are beneficial for society, particularly with regard to enhanced food production, though other consequences of nutrient enrichment are detrimental. Many of these effects are linked to each other through various biogeochemical processes.

NITRATE IN FOOD AND DRINKING WATER

In agricultural systems, most N inputs come from fertilizer, manure, or the cultivation of leguminous crops. The potential environmental and human health consequences of N inputs in such systems can be found in numerous reviews (e.g. Galloway et al. 1995, Townsend et al. 2003). Some of the direct and indirect effects of N applications identified below have obvious beneficial or deleterious consequences. However, human health threats posed by elevated nitrate levels in drinking water and foodstuff are still controversial.

When drinking water containing high amounts of nitrate or when eating nitrate-rich food, nitrate is converted to nitrite in the mouth. The nitrite in turn can restrict haemoglobin's ability to transport oxygen resulting in methaemoglobinaemia (Townsend et al. 2003). Very limited research in the period from 1945 to the 60's suggested the first link between high nitrate contents in well water and methaemoglobinaemia. Recent research, however, points to the unhygienic conditions of well water possibly being a dominant factor in the earlier observations. The real problem may have been conversion of nitrate to (methaemoglobinaemia-inducing) nitrite by microorganisms, rather than the high nitrate content of the well water per se (L'hirondel & L'hirondel 2002).

Regarding potential threats to food safety, from a human nutrition perspective, the presence of nitrate in the body can come from via endogenous and external sources. The endogenous source refers to the cellular synthesis from the amino acid L-arginine. The external sources are derived from drinking water and food. The intake of nitrate in vegetables accounts for more than 80% of the nitrate ingested by humans in the USA and 60% in the UK. Nitrate concentrations in vegetables vary widely according to species, maturity, fertilization and light intensity, but mean values can reach >2500 mg NO₃^-/kg. The high concentrations of plant nitrate are associated with excessive applications of mineral fertilizers or manure, although the relationship is neither very close nor systematic (Greenwood & Hunt 1986). Drinking water usually provides only a minor portion (2-25%) of the body's external intake of nitrate (L'hirondel & L'hirondel 2002).

Nitrate has been linked to stomach cancer since 1970. It was believed that cancer was induced by the nitrosamines formed as the result of nitrite reacting with amines. However, extensive research has failed to conclusively identify nitrate as the cause of increased risk of cancer (L'hirondel & L'hirondel 2002). In fact, recent studies have shown a number of significantly positive aspects of the presence of nitrate in water or food (Jenkinson 2001). It has been demonstrated that both nitric oxide (NO) and peroxynitrite (ONOO^-) can be formed in the human body from nitrate. Both compounds have an antifungal and antibacterial effect against organisms such as Salmonella, E. coli and Helicobacter pylori. Other studies also suggest that nitrate protects against cardio-vascular diseases. The research on the beneficial effects of dietary nitrate is already very promising (Addiscott & Benjamin 2004).

ACIDIFICATION OF THE ENVIRONMENT

Potentially the most important local impact of fertilizer N is related to the risk of soil acidification. The application itself of reduced, inorganic N in certain fertilizers (urea or anhydrous ammonia) or following ammonification of organic matter (such as legume residues) does not directly lead to soil acidification. To contribute to soil acidification, ammonium must be nitrified to form nitrate, and then nitrate and associated cations must subsequently be leached down the soil profile. In contrast, the application of ammonium-based fertilizers (ammonium nitrate, ammonium phosphate or ammonium sulfate) increases the net H⁺ concentration of soils, and thus directly contributes to soil acidification even in the absence of nitrate leaching. Soils can also acidify indirectly. Indeed, increased crop productivity leads to an enhanced rate of cation removal in agricultural production. So, although acidification of soils is a natural process it tends to be accelerated with increased N inputs. If lime is not regularly applied over a long enough period, crop performance will ultimately be reduced through various ways, including aluminum and manganese toxicities and reduced availabilities of numerous essential nutrients (Crews & Peoples 2004).

GREENHOUSE EFFECT, DESTRUCTION OF STRATOSPHERIC OZONE AND TROPOSPHERIC OZONE

Of the four major N gases (NO, NO₂, N₂O and NH₃) released into the atmosphere as a consequence of human activities, agriculture is believed to be a major source of two of them, NH₃ and N₂O (Jenkinson 2001). A survey of the most important greenhouse gases and their characteristics is given in Table III. According to Peoples et al. (2004), health and environmental implications associated with gaseous forms of N include: (1) respiratory and cardiac diseases, (2) formation of hydroscopic aerosols leading to acid deposition and decreased visibility, (3) depletion of stratospheric ozone by N₂O emissions, (4) formation of tropospheric ozone, (5) ozone-induced injury to crop, forest and natural ecosystems, (6) increased productivity of N-limited natural ecosystems following N deposition and N saturation of soils in forests and other natural ecosystems, (7) acidification and eutrophication effects on forests and soils, (8) biodiversity changes in terrestrial ecosystems, (9) changes in botanical composition and (10) invasion by 'weedy' species.

Nitrous oxide is a potent greenhouse gas, with a long half-life in the atmosphere (110-150 years, Peoples et al. 1995). Emissions of NO and NO₂ into the atmosphere contribute to acid deposition, which load atmospheric acid to the ecosystems in the forms of gases, particles, and liquid. Both lead to air pollution through production of other photochemical oxidant species in the atmosphere such as ozone.

EUTROPHICATION

Many of the world's surface waters are moderately to severely degraded from nutrient pollution, and because N is typically a limiting nutrient (especially in estuarine environments), it plays a critical role (Vitousek et al. 1997). Excessive loadings of nutrients (mainly N and P) to both fresh and coastal waters can result in eutrophication. This results in rapid growth of blue-green algae and macrophytes, depletion of oxygen in surface water, disappearance of aquatic biodiversity, and production of toxins which are poisonous to fish, cattle and humans (Rabalais 2002).

Many N budget studies have shown that there is a direct and positive correlation between total net N inputs to landscapes and riverine N export, whether considered at the scale of small watersheds, large river basins (Boyer et al. 2002), or regional drainage areas (Howarth et al. 2002). Major drivers behind the N increase in surface waters are the increasing N inputs to landscapes, from population growth, agricultural intensification, and atmospheric N deposition from fossil fuel combustion (Boyer et al. 2004). Inputs of N to surface waters have grown significantly in many parts of the world as human activities have increased N inputs to landscapes (Howarth et al. 2002). A study of all of the major watersheds draining to the North Atlantic Ocean indicates that N fluxes have increased 2- to 20- fold since pre-industrial times, directly proportional to increases in N inputs to these regions which are dominated by fertilizer use and atmospheric deposition (Howarth et al. 1996).

CONCLUSIONS

No doubt the use of synthetic N fertilizers and incorporation of N fixing plants in cropping systems have led to more and better food worldwide. Knowledge of the influence of agricultural activities on N cycling has tremendously increased during the last decades. However, only lately more emphasis has been put on processes whereby N is lost from the soil-plant system and influences the environment. Interaction of these processes is complex and needs further research. Because effects are situated at local (field), regional, national and continent levels, further study of its impact and health consequence should be given priority.

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Received 07/02/05
Accepted 14/06/05