《森林生态学》课程教学资源（生态学热点）Issues in ecology - 15 环境中过量的氮 Excess Nitrogen in the U.S. Environment：Trends, Risks, and Solutions.pdf_大学文库

© The Ecological Society of America • esahq@esa.org esa 1 ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 Excess Nitrogen in the U.S. Environment: Trends, Risks, and Solutions SUMMARY I t is not surprising that humans have profoundly altered the global nitrogen (N) cycle in an effort to feed 7 billion people, because nitrogen is an essential plant and animal nutrient. Food and energy production from agriculture, combined with industrial and energy sources, have more than doubled the amount of reactive nitrogen circulating annually on land. Humanity has disrupted the nitrogen cycle even more than the carbon (C) cycle. We present new research results showing widespread effects on ecosystems, biodiversity, human health, and climate, suggesting that in spite of decades of research quantifying the negative consequences of too much available nitrogen in the biosphere, solutions remain elusive. There have been important successes in reducing nitrogen emissions to the atmosphere and this has improved air quality. Effective solutions for reducing nitrogen losses from agriculture have also been identified, although political and economic impediments to their adoption remain. Here, we focus on the major sources of reactive nitrogen for the United States (U.S.), their impacts, and potential mitigation options: Sources: • Intensive development of agriculture, industry, and transportation has profoundly altered the U.S. nitrogen cycle. • Nitrogen emissions from the energy and transportation sectors are declining, but agricultural emissions are increasing. • Approximately half of all nitrogen applied to boost agricultural production escapes its intended use and is lost to the environment. Impacts: •Two-thirds of U.S. coastal systems are moderately to severely impaired due to nutrient loading; there are now approximately 300 hypoxic (low oxygen) zones along the U.S. coastline and the number is growing. One third of U.S. streams and two fifths of U.S. lakes are impaired by high nitrogen concentrations. • Air pollution continues to reduce biodiversity. A nation-wide assessment has documented losses of nitrogensensitive native species in favor of exotic, invasive species. • More than 1.5 million Americans drink well water contaminated with too much (or close to too much) nitrate (a regulated drinking water pollutant), potentially placing them at increased risk of birth defects and cancer. More research is needed to deepen understanding of these health risks. • Several pathogenic infections, including coral diseases, bird die-offs, fish diseases, and human diarrheal diseases and vector-borne infections are associated with nutrient losses from agriculture and from sewage entering ecosystems. • Nitrogen is intimately linked with the carbon cycle and has both warming and cooling effects on the climate. Mitigation Options: •Regulation of nitrogen oxide (NOX) emissions from energy and transportation sectors has greatly improved air quality, especially in the eastern U.S. Nitrogen oxide is expected to decline further as stronger regulations take effect, but ammonia remains mostly unregulated and is expected to increase unless better controls on ammonia emissions from livestock operations are implemented. • Nitrogen loss from farm and livestock operations can be reduced 30-50% using current practices and technologies and up to 70-90% with innovative applications of existing methods. Current U.S. agricultural policies and support systems, as well as declining investments in agricultural extension, impede the adoption of these practices. Society faces profound challenges to meet demands for food, fiber, and fuel while minimizing unintended environmental and human health impacts. While our ability to quantify transfers of nitrogen across land, water, and air has improved since the first publication of this series in 1997, an even bigger challenge remains: using the science for effective management policies that reduce climate change, improve water quality, and protect human and environmental health. Cover photo credit: Nitrogen deposition at the Joshua Tree National Park in California has increased the abundance of exotic grasses, which are more prone to fire than native vegetation. The upper photo shows a site dominated by exotic annual grasses five years after a burn, and the lower shows a site immediately post-burn. Photos courtesy of Edith Allen

2 esa © The Ecological Society of America • esahq@esa.org Introduction Thanks largely to the early 20th century invention of synthetically manufactured nitrogen (N) fertilizers, the growing human population is, on average, better nourished now than ever before in human history. About 40 to 60% of the current human population depends upon crops grown with synthetic nitrogen fertilizer. Unfortunately, this impressive advance in agricultural productivity and human nutrition has come at a high price of environmental degradation and human health risks from pollution. A large fraction of nitrogen fertilizer applied to cropland – often over half – is not used by the crops and is lost to air, water, and downstream and downwind habitats, polluting landscapes and waterscapes. At the same time, energy, transportation, and industrial sectors also emit nitrogen pollution into the air through increasing use of fossil fuels. In 1997, the first Issue in Ecology described the magnitude, causes, and consequences of these human alterations of the nitrogen cycle, documenting how humans have more than doubled the amount of reactive nitrogen (see Glossary for definitions) annually in circulation in the terrestrial biosphere. Several of these trends have continued along with increasing numbers of people, including improving human diets in the developing world, increasing global use of fertilizers, increasing atmospheric concentrations of the potent greenhouse gas nitrous oxide, and increasing eutrophication of aquatic and terrestrial habitats. Fifteen years later, we now ask: “Has scientific awareness of the growing problems of nitrogen pollution fostered progress in finding solutions?” In some respects, the answer is a disappointing “no.” Atmospheric nitrous oxide is still increasing, the number of aquatic ecosystems experiencing eutrophication and hypoxia (low oxygen waters) has grown, and biodiversity losses due to air pollution have continued. Indeed, these problems have been exacerbated by unanticipated new demands for biofuel crops, which created further demand for agricultural expansion and fertilizer inputs. Yet there have been important success stories. Significant air quality improvements are the result of regulations and technological innovations that have reduced nitrogen emissions from industry and automobiles in many developed countries. The amount of nitrogen in air pollution that some ecosystems can sustain (the “critical load”) without significant loss in diversity or ecosystem function has been estimated. Progress has also been made on improving the efficiency of fertilizer use and on identifying effective management options to reduce nitrogen losses from agricultural lands. Evidence of the links between excess reactive nitrogen in the environment and specific human health outcomes is growing, providing compelling motivation for pollution abatement. Perhaps the most encouraging aspect of progress in reducing nitrogen pollution is that technological solutions do exist. Research is needed to reduce costs of these solutions, and better communication is needed to foster the cultural and political will to apply them. While the nitrogen cycle disruption is global, the impacts are often felt locally, and the solutions are region-specific. Here, we focus on the major sources of reactive nitrogen for the U.S., their impacts on ecosystems, climate, and human health, and options to minimize nitrogen losses and impacts. The Major Anthropogenic Sources Of Reactive Nitrogen In The U.S. For the U.S., the combined anthropogenic sources of reactive nitrogen are about four times larger than natural sources of inputs from biological nitrogen fixation (see Glossary for Excess Nitrogen in the U.S. Environment: Trends, Risks, and Solutions Eric A. Davidson, Mark B. David, James N. Galloway, Christine L. Goodale, Richard Haeuber, John A. Harrison, Robert W. Howarth, Dan B. Jaynes, R. Richard Lowrance, B. Thomas Nolan, Jennifer L. Peel, Robert W. Pinder, Ellen Porter, Clifford S. Snyder, Alan R. Townsend, and Mary H. Ward ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012

© The Ecological Society of America • esahq@esa.org esa 3 ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 definitions) in native ecosystems and from lightning (Table 1). Because of intensive agricultural and industrial development, the alteration of the U.S. nitrogen cycle is greater than the global average. While nitrogen fertilizer use is growing in emerging-market regions such as Asia, it has nearly leveled off in the U.S. Soybean production has been increasing, which increases biological nitrogen fixation in croplands. Nitrogen oxide (NOX) emissions have declined and are expected to decline further. In addition to the annual inputs of newly fixed reactive nitrogen shown in Table 1, the redistributions and transfers of nitrogen across landscape components are also important (Figure 1). These include ammonia, nitrogen oxides and nitrous oxide emissions from soils to the atmosphere, leaching of nitrate and dissolved organic nitrogen from land to water, food harvests, and sewage disposal. This movement of reactive nitrogen into air, water, and nonagricultural land leads to unintended, mostly undesirable consequences for ecosystem and human health. A 2011 EPA report (see suggestions for further reading) describes these estimates in more detail. Our emphasis here will be in describing and quantifying impacts on human and ecosystem health and potential solutions. IMPACTS ON ECOSYSTEMS Research during the last few decades has led to an improved understanding of the relationship between nitrogen inputs and nitrogen demand by plant communities. Nitrogen generally enhances the growth of plants, but plant species differ in their ability to respond to increased nitrogen, due to variation in their inherent growth rates and their responses to other associated changes, such as acidification and nutrient imbalances. Many native hardwood tree species in the eastern U.S., such as red and sugar maple, white ash, black cherry, tulip poplar, and red oak, respond positively to nitrogen deposition from air pollution, whereas beech and several birch and oak species show no growth response. Conifer responses are mixed, with several species, particularly red pine, showing reduced growth with increasing nitrogen deposition (Figure 2). In addition to effects on trees, the understory vegetation is often particularly susceptible to changes in species composition due to increasing nitrogen deposition. Trees grow slowly where soils are thin and the growing season is short, for example in the Rocky Mountains. Field research has shown that much less nitrogen deposition is needed to satuFigure 1. The most important transfers and redistributions of reactive nitrogen among landscapes and waterscapes (see Glossary for abbreviations). Biological nitrogen fixation, denitrification, and a few minor transfers are omitted for visual simplicity. Table 1. Estimates of the major sources of natural and anthropogenic N inputs to the United States in 1990 and 2008 and projections for 2014. U.S. Nitrogen Sources 1990 2008 2014 Projection Millions of metric tons N per year Natural sources Lightning 0.1 0.1 0.1 Biological N fixation 6.4 6.4 6.4 Agriculture Synthetic N fertilizer 9.7 11.4 11.9 Crop biological N fixation 5.4 8.3 9.1 Food imports 0.2 0.2 0.2 Combustion Industrial NOX 1.5 1.1 1.1 Transportation NOX 3.7 2.6 2.0 Electric generation NOX 1.8 0.8 0.6 Industrial uses* 4.2 4.2 4.2 TOTAL 34.0 35.2 35.8 *Industrial uses of synthetic reactive N include nylon production and munitions. The only estimate available is for 2002, which we assume is constant for this time period for lack of better data. Sources include EPA reports and datasets (EPA-SAB-11-013, EPA-HQ-OAR-2009-0491, http://www.epa.gov/ttnchie1/trends/) and the International Fertilizer Industry Association

ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 rate the plant demand in high elevation forests compared to low elevation forests. Much of the nitrogen that is not taken up by the plants then enters streams, groundwater, and lakes, where it affects algal productivity and aquatic food webs. This type of research throughout the country is leading to estimates of “critical loads” of nitrogen deposition calculated for each ecosystem type and location (see Box 1). In addition to supplying an essential plant nutrient, nitrogen deposition also affects soil properties. Both nitrogen and sulfur from air pollution contribute to the acidification of soils, which leads to the loss of essential plant nutrients, such as calcium and magnesium, and alters the availability of phosphorus. Soil acidification mobilizes elements like aluminum, which is toxic to many plants on land and to many fish and other fauna in streams and lakes. Acidification of soils can increase forest susceptibility to disease and drought by stressing plants. Air polluted with nitrogen is often accompanied by ozone pollution, which suppresses plant photosynthesis. Species vary in their ability to tolerate these stresses from air pollution. Species-specific responses to elevated nitrogen deposition have reduced the diversity of terrestrial and aquatic ecosystems. In general, fast growing, “weedy” species, many of which are non-native, respond quickly and positively to increased nitrogen deposition, whereas slow-growing native species that are adapted to naturally low levels of nitrogen are less able to use the additional nitrogen. The differing responses can drive local populations of rare, slow-growing, native plant species 4 esa © The Ecological Society of America • esahq@esa.org Figure 2. Nitrogen deposition from air pollution increases the growth of many hardwood tree species, such as the red maple (left). Some conifers, such as red pine (right), show a decreased growth rate. Responses of the 24 most common species in the eastern U.S. can be found in Thomas et al. 2010. Nature Geoscience, 3:13-17. Figure 3. In California, airborne nitrogen is impacting one third of the state’s natural land areas. Lichens and stream nitrate concentrations have been used as effective indicators of undesirable changes in ecosystems. Areas shaded in red indicate conifer forests at risk because inputs from nitrogen in air pollution are exceeding the estimated critical load, either because (a) the species of lichen is expected to change or (b) nitrate in stream water is expected to exceed an established threshold value. Green shading indicates areas where pollution inputs are less than the critical loads. Redrawn from Fenn et al. (2010. Journal of Environmental Management 91:2404-2423), where critical load exceedance maps for additional California ecosystems can be found

© The Ecological Society of America • esahq@esa.org esa 5 ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 to extinction. The herbivores that feed on these plants are also affected. For example, checkerspot butterfly populations in serpentine grasslands of California have declined following replacement of native with invasive nitrogenloving grasses. In other cases, herbivore populations expand when the plants they feed upon become enriched with higher tissue concentrations of nitrogen, and lower concentrations of defensive chemicals. The expansion of nitrogenloving, non-native, highly flammable grasses in the western U.S. has increased fire risk. (e.g., see cover photos) Much of the reactive nitrogen in terrestrial ecosystems that is not taken up by plants or retained in soils ends up in aquatic ecosystems. Roughly two-thirds of U.S. coastal systems have recently been classified as moderately to severely impaired due to nutrient loading. Overenrichment with nitrogen is associated with increased frequency, severity, and extent of hypoxic (low oxygen) and anoxic (no oxygen) events, harmful and nuisance algae blooms, and species shifts leading to biodiversity loss. An increase in occurrence of coastal hypoxic and anoxic zones has been reported every decade since the early 1900s, with nearly 300 hypoxic zones along the U.S. coastline. In New England estuaries, phytoplankton (microscopic algae) now dominate over native sea grasses, resulting in aquatic ecosystems with much less structural complexity and lower water clarity. Enrichment of nitrogen in freshwaters often has negative impacts similar to those seen in coastal waters, and also affects drinking water quality (see human health impacts section). Although plant and algal growth in freshwater systems is strongly constrained by phosphorus (P), there is considerable evidence for co-constraints by both nitrogen and phosphorus. Recent surveys carried out by the EPA indicate that roughly one-third of the total stream length in the U.S. is considered “most disturbed” with respect to total nitrogen concentrations, and roughly one-fifth of all U.S. lakes are ranked poor with respect to total nitrogen concentrations. IMPACTS ON CLIMATE The importance of the nitrogen cycle in regulating climate is gaining increasing attention. Early global climate models focused solely on the physics of greenhouse gas effects; later models incorporated biological sources and sinks of carbon dioxide, but did not include carbon-nitrogen interactions. In recent years, a few earth system models have added some representation of the nitrogen cycle as a crucial regulator of the carbon (C) cycle, climate, and atmospheric chemistry, but the representation of nitrogen cycling processes in climate models remains far from complete. Deposition of airborne reactive nitrogen onto land affects terrestrial carbon sinks through two key processes. First, inputs of nitrogen often increase the growth of trees, which store high amounts of carbon in their wood. The magnitude of growth stimulation is of some debate, but is likely greatest in regions of moderate nitrogen deposition. Increasing atmospheric carbon dioxide concentrations also stimulate plant growth, but this stimulation is constrained by the availability of nitrogen to plants. Second, inputs of reactive nitrogen slow breakdown of dead plant material and soil organic matter in many, but not all forest soils. Why nitrogen deposition slows these breakdown processes is an area of active research into changes in soil microbial communities, microbial biomass, and enzyme production needed to break down complex organic matter. The most direct effect of nitrogen on climate is through nitrous oxide, the third most important anthropogenic greenhouse gas, contributBox 1. CRITICAL LOADS: HOW MUCH NITROGEN IS TOO MUCH? Excess nitrogen can disrupt natural ecosystems, causing acidification, nutrient imbalances, and loss of biodiversity. To manage nitrogen effectively, it is important to know how much nitrogen can be added to an ecosystem without provoking harmful effects. The term “critical load” describes how much nitrogen is too much. Critical loads usually refer to nitrogen deposited from air pollution and are expressed as loading rates of nitrogen in a given area over time, usually as kilograms of nitrogen per hectare per year. They are widely used in Europe and Canada to evaluate how nitrogen, sulfur, and other air pollutants affect streams, lakes, and forests, and are now being developed for ecosystems in the U.S. Maps of critical loads are combined with maps of air pollution to show where pollution loads exceed the estimated local critical load, putting ecosystems at risk. For example, in California, maps of critical loads combined with actual nitrogen loads highlight areas where nitrogen is likely affecting forests (Figure 3), grasslands, coastal sage, desert, and streams. This information helps air quality managers determine where and how much air quality needs to be improved, in order to reduce excess nitrogen loadings and to restore harmed areas

ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 6 esa © The Ecological Society of America • esahq@esa.org ing 6% of total human-induced global warming. It has about 300 times the per-molecule warming potential of carbon dioxide and is long-lived in the atmosphere (a “mean residence time” of more than 110 years). Atmospheric concentrations of nitrous oxide have increased rapidly since 1860, as livestock herds increased globally and as use of synthetic-nitrogen fertilizers increased after World War II. The EPA estimates that agricultural activities are directly or indirectly responsible for emissions of 0.48 million tons of nitrogen as nitrous oxide per year, which is about 80% of total U.S. nitrous oxide production (the remainder is from energy and industrial sources) and about 10% of the global nitrous oxide emissions from agriculture. Reactive nitrogen also affects methane, another important greenhouse gas, through chemical reactions that destroy atmospheric methane and through inhibition of methane production and consumption by microbes in soils and wetlands. However, the overall climate impacts of reactive nitrogen via methane are small compared to those of nitrous oxide and carbon sequestration. While not greenhouse gases directly, nitrogen oxides often affect the production of ozone in the troposphere (the lower atmosphere). Ozone affects climate directly as a greenhouse gas, and it is also toxic to plants, decreasing photosynthesis and plant uptake of atmospheric carbon dioxide by as much as 20%. Both nitrogen oxides and ammonia affect the formation of tiny airborne particles, also known as aerosols, and their chemical properties. The abundance and properties of these particles influence the formation of cloud droplets. In some cases this causes clouds to be brighter and longer-lived, which has important effects on precipitation and temperature patterns. Overall, aerosols have a short-term cooling effect, but the long-term effect is small because the aerosols are frequently washed out of the air by rain. The above discussion of the impacts of reactive nitrogen on climate is global in scope, not U.S.-specific. Efforts are underway to create a U.S.-specific nitrogen assessment, with preliminary findings shown in Figure 4. It compares the long-term warming potentials of nitrogen gases and particulates and carbon sequestration attributable to U.S. emissions of reactive nitrogen. The cooling effects of nitrogen deposition through carbon sequestration roughly cancel the warming effect of nitrous oxide (Figure 4). Putting these estimates into a broader perspective, these contrasting warming and cooling effects of nitrogen are equivalent to less than 10% of the warming effect of U.S. emissions of carbon dioxide from fossil fuel combustion. IMPACTS ON HUMAN HEALTH Drinking water and human health Nitrate concentrations in groundwater are increasing in many parts of the U.S., raising concerns for human health, particularly in rural agricultural areas where shallow groundwater is often used for domestic water supplies. The EPA’s maximum contaminant level (MCL) for public drinking water supplies is 10 milligrams per liter as nitrate-nitrogen (or about 45 milligrams per liter as nitrate). Nitrate concentrations above the MCL are relatively uncommon in streams and deep aquifers used for drinking water supplies. However, the MCL was exceeded in 22% of shallow (less than 100 feet below the water table) domestic wells in agricultural areas, an increase from a decade earlier, according to a 2010 U.S. Geological Survey (USGS) report. Taking into account the regional sources of nitrate and regional differences in geology that affect its movement to groundwater, the USGS study shows large areas in agricultural and urban regions with shallow groundwater nitrate exceeding 10 milligrams nitrogen per liter (Figure 5). Based on a USGS model of drinking water quality, it is estimated that about 1.2 million Americans use private drinking wells with nitrate concentrations between 5 and 10 milligrams nitrogen per liter, and about a half million Americans use wells that exceed the MCL of 10 milligrams nitrogen Figure 4. The cooling effects resulting from U.S. nitrogen deposition (which allows trees to remove carbon from the atmosphere and causes reflection of the sun by nitrogen-containing haze and particles in the air) slightly outweigh the warming effect of U.S. nitrous oxide emissions. However, uncertainties in these calculations are large, yielding the following ranges of estimates: +180 to +400 for N2O; -240 to -540 for tree growth; and -2 to -16 for haze, where positive numbers indicate warming and negative numbers cooling. Because various different greenhouse gases and aerosols are included in this analysis, all are converted to the common currency of “CO2-equivalents” on a 100-year global warming potential time frame, using the methodologies of the Intergovernmental Panel on Climate Change

© The Ecological Society of America • esahq@esa.org esa 7 ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 per liter. Future contamination of deeper groundwater pumped from public supply wells is a growing concern due to increasing nitrate concentrations of deep aquifers resulting from downward transit of shallow groundwater. The EPA and World Health Organization drinking water standards were set to prevent methemoglobinemia in infants, also known as “blue baby syndrome.” Methemoglobinemia is uncommon in the U.S. due, in part, to adherence to the standards in most areas. However, other health conditions have been linked to nitrate ingestion. About 5% of ingested nitrate is converted by bacteria in the mouth to nitrite, which then forms several compounds with different effects in the body. In the acidic stomach, nitrite forms nitric oxide, which lowers blood pressure, providing a beneficial effect. Nitrite also reacts with amines and amides, present in proteins from the diet or from medications, to form N-nitrosamines and N-nitrosamides (collectively N-nitroso compounds; see Figure 6). These compounds damage DNA and have been shown to cause birth defects and cancer in animals. Because all animal species tested so far have been susceptible to cancer induced by Nnitroso-compounds, it is likely that humans are also affected. However, well-designed human studies that include factors affecting N-nitroso-compound formation in the body are few, limiting the ability to draw definitive conclusions about cancer risk at this time. Nevertheless, the UN World Health Organization International Agency for Research on Cancer expert working group concluded: “Ingested nitrate or nitrite under conditions that result in endogenous nitrosation is probably carcinogenic to humans” (endogenous nitrosation refers to the formation of N-nitrosocompounds in the stomach, as described above). Increased risks for stomach, esophageal, colon, and kidney cancer have been found in the few studies that have evaluated people with high intake of nitrate from drinking water or diet and low intake of vitamin C. The production of N-nitroso-compounds is decreased by vitamin C and other compounds in fruits and vegetables and increased by heme iron in red meats, so the risk could be minimized by a diet rich in fruits and vegetables and worsened by a diet rich in red meat. In addition to cancer risks, high nitrate concentrations in drinking water supplies have been linked to increased risk of spontaneous abortions, premature births, and intrauterine growth retardation, although not all studies found these associations. In four studies to date, central nervous system malformation has been linked to the nitrate in drinking water of pregnant women, including some evidence at nitrate concentrations below the EPA standard. High levels of nitrate ingestion via drinking water were associated with increased rates of thyroid enlargement (hypertrophy) and thyroid underfunction (hypothyroidism). Given these findings, more research is needed to evaluate the range of health effects due to nitrate ingestion. Air pollution and human health A growing body of evidence demonstrates that some nitrogen-related air pollutants are hazardous for human health (Table 2). Nitrogen oxide is an important component of outdoor and indoor air pollution. Nitrogen oxide is emitted by automobiles, electrical power plants, and construction machinery. Tailpipe emissions make up the majority of urban sources; minor natural sources include lightning, soil emissions, and wildland fires. Nitrogen oxide reacts with other components of air pollution to form ozone and several constituents of fine particulate matter. Particulate matter is a mixture of solid and liquid particles that Figure 5. A U.S. Geological Survey model for shallow groundwater predicts moderate (yellow and orange) to severe (red) nitrate contamination in areas with large nitrogen sources and where the geologic features allow the nitrate to reach the groundwater. Redrawn from USGS Circular 1350 by Dubrovsky et al. (2010)

ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 8 esa © The Ecological Society of America • esahq@esa.org vary in size and chemical composition, often containing ammonium and/or nitrate. Particulate matter that is less than 2.5 microns in diameter, PM2.5, penetrates and deposits in the lungs, causing the most harm. Using 2005 air pollution data, EPA analysts estimated that PM2.5 exposure caused 130,000 annual premature deaths in the U.S. and ozone exposure caused another 4,700. It is estimated that these pollutants spur hundreds of thousands of hospital visits and millions of additional respiratory symptoms each year in the U.S. For the regulated pollutants shown in Table 2, populations at increased risk include those with pre-existing cardiovascular and respiratory conditions, developing fetuses, infants, children, and the elderly. Outdoor work or physical exertion, lifestyle (e.g., poor nutrition), low socio-economic status, and genetic predisposition also increase risks. It is possible that these pollutants could interact with each other or with other pollutants to produce health effects, but current regulatory and research frameworks do not address the effects of multi-pollutant atmospheres. Figure 6. N-nitroso-compounds (NOCs) damage DNA and cause birth defects and cancer in animals. There is a need for more well-designed human studies to draw stronger conclusions about cancer risk from nitrate and nitrite ingestion. Table 2. Summary of evidence for links between N-related air pollutants and human health. Pollutant and Scientific Assessment Evidence Suggests A Clear Link Probable Link (More Evidence Needed) NOx (typically measured as NO2) Short-term* respiratory disease, including: Short-term increased risk of death from • increased lung inflammation and sensitivity, respiratory and heart disease 2008 EPA Integrated particularly among asthmatics Science Assessment (ISA) • increased wheezing, coughing, and asthma Long-term* respiratory disease, including: symptoms • decreased lung function • increased hospital visits for asthma and • decreased lung growth and function in children other respiratory ailments Ozone Short-term respiratory disease, including: Short-term heart disease, including: • increased hospital visits • increased hospital visits 2006 EPA Air Quality • increased lung inflammation and sensitivity, • decreased heart function Criteria Document particularly among asthmatics (AQCD) • increased wheezing, coughing, and asthma symptoms Short-term increased risk of death from respiratory and heart disease PM2.5 Short-term and long-term heart and respiratory Adverse reproductive outcomes, such as: disease, including: • increased risk of preterm birth 2009 EPA Integrated Science • increased hospital visits • decreased birth weight Assessment (ISA) for PM • decreased heart and lung function • increased risk of infant mortality Short-term and long-term increased risk of Long-term increased risk of cancer death from respiratory and heart disease * Short-term refers to days or weeks between exposure of the pollutant and onset of health symptoms. Long-term refers to months or years

© The Ecological Society of America • esahq@esa.org esa 9 ISSUES IN ECOLOGY NUMBER FIFTEEN WINTER 2012 Effects on human health through wildlife In contrast to toxicological diseases such as blue-baby syndrome, most emerging human infectious diseases are zoonotic, meaning they depend on wildlife as hosts, vectors, or reservoirs. As a result, understanding the factors that contribute to zoonotic diseases requires an ecological approach that recognizes the linkages among environmental change, pathogen transmission, and human and nonhuman hosts. Nutrient runoff and the concentrations of nitrogen, phosphorus, and organic matter have frequently been associated with a wide range of pathogenic infections, including coral diseases, bird die-offs, diarrheal diseases, vector-borne infections, and fish diseases. Experimental studies have helped to identify the ways that nitrogen exacerbates disease, including changes in host or vector density, host distribution, infection resistance, pathogen virulence or toxicity, and the increases in resources to the pathogen. For example, West Nile virus was first introduced to the U.S. in 1999 and has since spread across North America through bird hosts and mosquitoes. The mosquito vectors of West Nile virus, including wetland-breeding species such as Culex tarsalis, increase egg laying and larval growth rates in response to nutrient enrichment. Several plausible but undocumented effects of nitrogen enrichment of ecosystems merit further study, including greater toxicity of harmful algal blooms, increases in allergy-provoking pollen from weedy plants like ragweed, and more favorable conditions for snails that harbor the fluke parasite that causes swimmer’s itch. MITIGATION OPPORTUNITIES IN AGRICULTURE The challenge of supplying sufficient nitrogen to crops has figured prominently in the development of agriculture. Since the time of Aristotle, farmers valued legumes for their ability to restore and maintain soil fertility, although the role of legumes in fixing nitrogen was not known until the 19th century. At that time, supplemental nitrogen sources such as Chilean saltpeter (sodium nitrate) and bat guano also came into use. Nevertheless, the lack of nitrogen often kept crop yields low. It was not until development of the HaberBosch synthesis process that nitrogen limitation was finally overcome for most of the world’s agriculture, although fertilizers are still often not available or affordable in subSaharan Africa. Synthetic nitrogen fertilizer use began in the U.S. following World War II, and rapidly increased during the 1960s and 1970s. Since then, nitrogen fertilizer consumption has increased only slightly each year, now approaching 12 million metric tons of nitrogen per year (Figure 7). Increased nitrogen fertilizer application has increased crop harvests, although improved soil conservation, nutrient, pest and water management, and crop varieties have also contributed to yield increases. These practices have contributed to overall improved fertilizer use efficiency. For example, corn yields have steadily increased at an average of 1.9% per year since 1960 (Figure 7), while nitrogen fertilizer average application rates to corn have remained relatively constant during the last 30 years at about 145 kg nitrogen per hectare. Despite improvements in crop production and nitrogen fertilizer efficiency, large losses of reactive nitrogen to the environment are still common from agricultural systems through transport of nitrate to groundwater or surface waters and through emissions of nitrogen gases to the air. Such nitrogen losses are especially common in regions where artificial subsurface drainage systems remove excess soil water from farms established on natural wetland areas. This loss is partly due to a timing problem. Large amounts of nitrate are present in the soil in the spring, but the crop either has not yet been planted or is still too small to take up much of the nitrogen, so that snow melt and spring rains often wash much of the nitrate away into groundwater and streams. Additional losses occur by release of ammonia, nitric oxide, and nitrous oxide gases to the atmosphere. Much of the U.S. crop production is fed to animals for meat and dairy production. Most livestock only utilize about 30% of the nitroFigure 7. U.S. fertilizer-N consumption rate increased rapidly in the 1960s and 1970s, but has since slowed to 0.6% per year since 1978 (blue circles and blue regression line). In contrast, average corn yield continues to increase at a rate of 1.9% per year (red diamonds and red regression line), indicating improved nitrogen use efficiency. Data from Association of American Plant Food Control Officials, The Fertilizer Institute, and the USDA National Agricultural Statistics Service (NASS)