Why the Global Change in Nitrogen Should Concern Us

The global change in carbon dioxide (CO2) has received considerable attention from the scientific and policy communities worldwide. Global warming, sea level rise, and changes in Earth’s patterns of precipitation are all now well recognized to be related to the changes in CO2 in the atmosphere. Scientists and policy makers have focused considerable effort in understanding the extent to which the change in CO2 may be related to man’s activities. From the efforts of thousands of individual scientists to the Intergovernmental Panel on Climate Change, which was awarded the Nobel Peace Prize with Al Gore, the consensus is overwhelming that man’s activities have resulted in an acceleration of the change in carbon in the Earth’s atmosphere. However, while media attention has been focused on global changes due to carbon, changes have occurred in another element, nitrogen, and these changes also have large global consequences. Nitrogen is a neighbor to carbon on the periodic table of elements and can be considered the secondary building block of life. The purpose of this paper is to describe how global nitrogen has been changed by man’s activities, and why, like carbon, it needs to be considered in the global change discussion.

Nitrogen is fundamental in every living organism. It is an essential element in protein, in nucleic acids (such as DNA), in chlorophyll, the green pigment of all plants, and in the enzymes which regulate biology and chemistry. About 80% of the atmosphere is made of nitrogen. Yet, most of this atmospheric nitrogen is in a non-reactive form - nitrogen gas - which is not available to most living organisms. Only selected organisms have the capability to convert or “fix” nitrogen gas into a reactive form that can then support life. Life cannot be supported without sufficient “fixed” nitrogen and thus the pathways by which nitrogen cycles through the oceans, terrestrial systems and atmosphere has been the focus of considerable study.

In the early 1900’s, an invention that could create the chemical “fixation” of nitrogen without using nitrogen-fixing organisms changed the Earth. This invention, for which Fritz Haber and Carl Bosch won Nobel Prizes, was motivated by the increasing recognition that nitrogen led to better crop yields. But, there was a limited supply of fixed nitrogen for farmers. Farmers knew that they would obtain better yields when they placed wood chips or Chilean guano on their fields, but availability of these natural ‘fertilizers’ was limited. Another motivation was the demand during World War I for explosives (ammunition) that required fixed nitrogen. Now known as the Haber-Bosch process, the seemingly simple chemical reaction of nitrogen gas and hydrogen to make ammonia, N2 + 3 H2 ? 2 NH3, is recognized as the “single most important change affecting the world’s population – its expansion from 1.6 billion people in 1900 to today’s 6 billion.”1 The invention of chemical nitrogen fixation, soon commercialized, led to rapid adoption of chemical fertilizers and the so-called ‘green revolution’ that has fed humanity.

The ability to grow food at an expanding pace escalated after World War II, fueled by the industrialization of nitrogen fixation. Prior to about 1960, biological nitrogen fixation from natural systems and legume crops contributed the largest source of “fixed” nitrogen to the Earth. Since then, industrial processes have contributed substantially more fixed nitrogen than supplied by biological processes (Fig. 1).2, 3 Now, in the US, industrial fertilizer contributes more than twice that of biological fixation; fertilizer use has quadrupled since 1960. In fact, half of all of the world’s chemical nitrogen fertilizer has been produced since 1985. The rate of increase in fertilizer consumption has increased even more rapidly in many parts of the developing world. China, for example, has increased its use of nitrogen fertilizer four-fold since the 1970’s alone, and together with the other countries of southeast Asia, use half of the world’s supply (Fig. 2). By comparison, the US now consumes only about 15% of the total world nitrogen fertilizer annually.4, 5 The use of other fertilizers, such as phosphorus, has also increased over the past decades, but the rate of increase in use of nitrogen far outpaces the rate of use of these other elements.6

Coincident with the escalating rate of use of nitrogen-based fertilizers, another change in fertilizer usage has occurred; a change in the chemical formulation of these fertilizers. Several decades ago, when fixed-nitrogen fertilizer use was just emerging, most of these fertilizers were in the chemical form of ammonium (NH4) or nitrate (NO3), often chemically combined with phosphate or sulfate. Now, most of these fertilizers are being produced in the chemical form of urea ((NH2)2CO).7 Worldwide use of urea as a nitrogen fertilizer and feed additive has increased tremendously in the past 4 decades (Fig. 3).8 Indeed, the 1990s were hailed as an “especially joyous time” for urea sales.9 Urea is now considered a commodity, and it is traded on the global market as such. Furthermore, industrial producers are continually seeking new uses or applications of their product. Global urea usage extends beyond agriculture; it is now used extensively in animal feeds, in manufacturing processes, and even as a road or airplane deicer.10

The increased use of nitrogen and, of course, phosphorus fertilizers have certainly been beneficial to humanity, providing the opportunity to increase food production, which, in turn, has supported growth in human population. It has been estimated that about 40% of the current growth in world population is due to increased food production from fertilized agriculture.11 Between 20-50% of all nitrogen fertilizer goes towards supporting feed for animals.12 The six billion people of the world share the planet with roughly 15 billion chickens, 1.5 billion sheep, 1.3 billion cattle, and 123 million lactating cows, as well as intensifying aquaculture industries.13 People and animals not only consume nitrogen through their foods and feed, but also generate large amounts of nitrogen in their waste. Of course, human waste, or sewage, is treated in the industrial world, although most treatment does not remove the nitrogen. Also, in vast parts of the developing world this waste is not treated at all. Moreover, animal waste is generally not treated either, and much is lost to the atmosphere in the form of gaseous ammonia. Many animal operations are now operated as confined or concentrated animal operations, or CAOs, which make their impact more localized and intensive. The transfer of fertilizer through agriculture to food is also extremely inefficient: about 14% of fertilizer nitrogen is consumed in food as vegetables, but only about 4% as meat; the rest is lost to the environment – to the atmosphere from volatilization, to groundwater, or to lakes, rivers and coastal waters from runoff.14

While the benefits of increased use of nitrogen for agriculture are clear, the consequences of a world containing altered nitrogen are also large. Eutrophication is one of the direst consequences. Eutrophication is the enrichment of coastal waters and lakes with excess nutrients, in turn leading to an increased growth of algae and a cascade of ecosystem consequences. The term eutrophication was formerly used mostly in reference to the natural aging of lakes wherein a large, deep, nutrient-poor lake eventually becomes more nutrient-rich, more productive with plant and animal life, and slowly becomes a pond, then a marsh.15 More recently, this term is now used almost exclusively in the context of the myriad effects of nutrient pollution. Many now consider nitrogen pollution to be the single greatest source of water pollution in lakes, rivers, and bays.16 The nitrogen that contributes to this eutrophication not only comes from agricultural runoff, but from sewage and waste from the expanding human and animal populations. Eutrophication can lead to loss of sea grasses and other habitats for fish and shellfish, coral reef destruction through algae overgrowth, development of low oxygen zones when algae begin to die, and the development of “Harmful Algal Blooms” or “HABs”. Zones of low oxygen are often referred to as “dead zones,” the largest of which in the US is in the Gulf of Mexico off of the Mississippi River plume, which drains the agricultural “bread basket” of the Midwestern states. Whether episodic or sustained, dead zones are responsible for losses of millions of dollars of commercial fish annually.17, 18, 19 Furthermore, the bacteria that proliferate in such dead zones may release methane or nitrous oxide to the atmosphere from their biological metabolism, in turn furthering greenhouse effects.

HABs are those proliferations of algae that can kill fish and shellfish in great numbers, produce toxins harmful to human health, and develop biomass accumulations that can alter ecosystems in other deleterious ways.20, 21 It is now well recognized that HAB events are growing in frequency, extent, and duration once they do occur, and that many of these events are the result of increasing eutrophication worldwide22, 23, 24. HABs produce a wide range of toxins, which may accumulate in predators and organisms higher in the food web ultimately affecting humans when seafood is consumed. HAB toxins may also affect humans when toxin-laden aerosols are inhaled, when contaminated water is consumed directly or, in some cases, when direct contact occurs through swimming. Toxic syndromes include paralytic, amnesic, diarrheic, and neurotoxic shellfish poisoning, and cyanotoxic poisoning, among others (Fig. 4).25 When certain types of these algae bloom in reservoirs their toxins can contaminate the water supply.26 Evidence is also mounting that more subtle effects are also being expressed in response to HABs by fish and wildlife. As an example, a neurotoxin produced by a toxic alga has been shown to induce seizure and memory loss in laboratory animals.27 In addition, sea lion mortalities are now common due to other types of toxic algae, and yet different toxic algae have been associated with embryonic deformities in oysters.28 In fact, more than 50% of marine mammal mortality events (deaths of marine dolphins, whales, sea lions and porpoise) are now linked to HABs.29 Fish kills are the most common wildlife effect of HABs, and may be directly due to toxicity or physical clogging of the gills by the algae, or indirectly due to dead zones that develop from algal bloom decay. HABs may also contribute to fish stress, making them more susceptible to other infections. Although not all HABs are directly related to increases in nitrogen loading, many are, and many of these algae also prefer nitrogen in the form of urea, the most commonly used commercial form of nitrogen.30 Not only is the proliferation of toxic dinoflagellate species associated with higher urea loading, but so too is the cellular toxin content of some HAB species.31, 32 Some freshwater HAB species have also been shown to increase their toxicity levels in the presence of excess nitrogen, a critical concern when these species proliferate in reservoirs.33, 34 Globally, the highest frequencies of occurrences of both HABs and coastal dead zones are in regions where both atmospheric deposition and riverine export of nitrogen is high, including Asia, Europe, and North America.35, 36, 37

The growth in human population, supported by increased agriculture, has led to other problems related to nitrogen. Acid rain is caused by the increased atmospheric emissions of numerous pollutants, including nitrogen compounds. Emissions of nitrogen from combustion of fossil fuels for energy generation and motor vehicles results in the formation of acidic compounds in the atmosphere which are deposited in rain (wet deposition) or which may become incorporated in dust or smoke and stick to the ground, trees, or buildings (dry deposition). In the atmosphere, nitrogen in the form of nitrous oxide contributes to the creation of greenhouse gases and the acidification of rainwater. Acid rain has been responsible for declines in forest health,38, 39 changes in species composition and losses of biodiversity,40, 41 acidification of soils42 and changes to the chemistry and radioactive (energy) balance of the atmosphere.43 Acid rain also contributes to the smog that pollutes many cities.44 Nitrogen enrichment of the atmosphere can also have direct effects on human health. Atmospheric enrichment of reactive nitrogen compounds, including nitric oxide, nitrate and nitrite, among other forms, can cause inflammation of the airways, and can be especially acute for those who suffer from asthma.

Another suite of consequences of the increased nitrogen loading to the world, and the resulting alteration of the global cycle of nitrogen, is an increase in the prevalence, severity, or distribution of human health problems and infectious diseases of both humans and wildlife in addition to those caused by HABs.45, 46, 47, 48 Direct health effects of nitrogen pollution come from several sources. Groundwater enriched with nitrate from fertilizers percolating from the soils above can cause hyperthyroidism, birth defects, and miscarriage. The concern is especially true for babies where excess nitrate in drinking water is linked to “blue baby syndrome”, which causes lack of oxygen to the brain.49 Reactive nitrogen compounds, which include nitric oxide, nitrate and some other compounds, as well as reactive oxygen compounds, have also been linked to the development of Parkinson’s disease in laboratory animal studies.50 Reactive nitrogen, because of its role in cell signaling, enzyme and protein synthesis and many other biological pathways, can also interfere, upon overexposure, with the enzyme reactions in cells that lead to age-related diseases.51

Nitrogen pollution is also indirectly related to the spread of several infectious diseases. Postulated mechanisms for these linkages include changes in host abundance and distribution, shifts in pathogen virulence, or changes in host susceptibility.52, 53 Vector-borne pathogens require a disease agent (e.g., a parasite), a vector (e.g., a mosquito) and a host. Changes in habitat as a result of altered nitrogen availability can affect any one of these roles.54, 55, 56 Mosquito-borne infections, for example, are often positively affected by inputs of nutrients to wetland breeding habitats.57 One specific example is West Nile Virus, which was introduced to the US in the late 1990’s. Experimental data has shown that the mosquitoes that carry the virus have up to ten times the numbers of eggs in nitrogen-rich compared to nitrogen–poor conditions58 and larval survival and the mean size of emerging adults are greater in treatments with higher nitrogen levels compared with control levels.59, 60 Other experimental data has shown that many parasites increase in abundance with low to moderate levels of eutrophication due to increased host density and an ability of the hosts to withstand infection under nitrogen-rich, compared to nitrogen-poor conditions.61, 62 It has also been suggested that SARS is related to the intensification of confined animal operations and the associated nitrogen pollution and change of suitable habitat for the virus.63

In summary, the increased use of nitrogen-based fertilizers has expanded in recent decades, with the positive outcome of increased food supplies and reducing global malnutrition. In fact, some parts of the world, such as sub-Saharan Africa, currently have rates of fertilizer application that are too low to sustain the agriculture needed for the population.64 Yet, the consequence of the excessive use of nitrogen is that global nitrogen cycles have been altered, causing increased eutrophication of both freshwater and marine waters, a changed ecology of both aquatic and terrestrial habitats, and the spread of infectious diseases. Moreover, the form of nitrogen that is now most commonly used, urea, may be exacerbating these effects in some sensitive coastal waters. The world’s human population is currently expected to continue to increase by 1-2% per year.65 Global fertilizer use is projected to double by the year 2080.66 Most of these increases are likely to occur in parts of the world that are already saturated with nitrogen and poorly prepared to deal with emerging diseases.

The relationships between the global biogeochemistry of nitrogen and the ecology of both plant and animal organisms that support both human food as well as human disease are complex, often nonlinear and indirect, and difficult to predict. These complexities and effects will be even greater in a warmer planet. As temperatures warm, precipitation patterns will continue to change. Higher precipitation rates, projected for some parts of the world, will lead to greater runoff and greater water pollution, requiring greater investments in coastal ecosystem management clean up and in drinking water purification. Warmer temperatures will also increase the rate at which nitrogen gases are volatilized to the atmosphere. There are economic, engineering, and environmental approaches that can be implemented to reduce our use of nitrogen without affecting food production. The increased production of corn for biofuels, which require nitrogen fertilizer for sustained production, is, unfortunately, not one of these solutions. It is time to recognize that carbon is not the only element that is changing and having a significant global impact. We have altered and will continue to alter the cycles of other elements as well with equally alarming consequences. paJ

About the Author:t Patricia M. Glibert is a Professor with the University of Maryland Center for Environmental Science, Horn Point Laboratory. She has worked on issues related to nitrogen cycling and nutrient pollution for more than 20 years. More information on her research can be found on her web site at: http://hpl.umces.edu/faculty/glibert/index.htm. She is a three-time parent of Hobart and William Smith students.

(Notes)

1. Smil, xiiv
2. Galloway and Cowling 2002
3. Howarth et al. 2002
4. Howarth et al. 2002
5. International Fertilizer Industry, www.fertilizer.org
6. Piccone and Van Tassel 2002
7. International Fertilizer Industry, www.fertilizer.org
8. Glibert et al. 2006
9. International Raw Materials, 2000
10. Glibert et al. 2006
11. Erisman 2007
12. Mooney 2007
13. Mooney 2007
14. Galloway and Cowling 2002
15. Wetzel 1983
16. Piccone and Van Tassel 2002
17. Joyce 2000
18. Diaz 2001
19. Mallin et al. 2006
20. Hallegraeff 1993
21. Glibert and Pitcher 2001
22. Anderson et al. 2002
23. Glibert et al. 2005
24. Glibert and Burkholder 2006
25. Landsberg 2002
26. Carmichael 2008
27. Tiedeken and Ramsdell 2007
28. Glibert et al. 2007
29. Ramsdell et al. 2005
30. Glibert et al. 2006
31. Shimizu et al. 1993
32. Leong et al. 2004
33. Stolte et al. 2002
34. Granéli and Flynn 2006
35. Galloway and Cowling 2002
36. Glibert et al. 2008
37. Diaz 2001
38. Schulze 1989
39. Aber et al. 1998
40. Vitousek et al. 1997
41. Stevens et al. 2004
42. Högberg et al. 2006
43. U.N. Intergovernmental Panel on Climate Change. www.ipcc.ch/
44. Vitousek et al. 1997a,b
45. Coyner et al. 2003
46. Rejmankova et al. 2006
47. Voss and Richardson 2007
48. Johnson et al. 2007
49. Majumdar 2003
50. Yokoyama et al. 2008
51. Drew and Leeuwenburgh 2002
52. McKenzie and Townsend 2007
53. Johnson and Carpenter 2008
54. Lawler and Dritz 2005
55. Yanoviak et al. 2006
56. Munga et al. 2006
57. Johnson et al., in review
58. Reiskind and Wilson 2004
59. Reiskind et al. 2004
60. Johnson et al., in review
61. Lafferty 1997
62. Johnson and Carpenter 2008
63. Millenium Ecosystem Assessment 2005
64. Galloway et al. 2002
65. Cohen 2003
66. Erisman 2007

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