Environmental Science Human Manipulation of the Global Nitrogen Cycle
by
Eve-Lyn S. Hinckley
  • LAST REVIEWED: 03 June 2019
  • LAST MODIFIED: 10 March 2015
  • DOI: 10.1093/obo/9780199363445-0023

Introduction

Ecosystems and all living beings are bathed in atmospheric N2, a nearly inert gas, which must be “fixed” by bacteria associated with plant roots or free-living in soil. These bacteria possess the enzyme nitrogenase, which allows them to convert N2 to reactive and bioavailable forms of N, including ammonium (NH4+) and nitrate (NO3-). N is a limiting nutrient in most ecosystems, so excess inputs of reactive N can have negative consequences, including changes to forest structure and function, and eutrophication of aquatic systems. Since the 1900s, humans have tripled the amount of reactive N cycling globally through air, land, and water systems. Both fossil fuel combustion and the advent of the Haber-Bosch process have contributed to accelerated N cycling. These hallmarks of modern society arose as a result of industrialization in the developed world and the pressure to produce synthetic N fertilizers that could support a growing human population. While they were considered great economic boons, these developments have had a cascade of unintended negative consequences for the biosphere. Combustion of fossil fuels releases N oxides into the atmosphere that can be transported large distances from their sources and cause acid rain and fertilization of downgradient terrestrial and aquatic systems. Widespread application (and over-application) of synthetic N fertilizers has caused increases in production of greenhouse gases (e.g., nitrous oxide) locally in croplands, and pollution of downgradient aquatic ecosystems from N-rich runoff. This article addresses the topic of human manipulation of the N cycle in a variety of ecosystems, as well as a number of specific locations around the globe. It does not serve as a general introduction to the N cycle. Those readers looking to start with the basics of N cycling, and biogeochemistry more generally, should see W. H. Schlesinger’s article on Biogeochemistry in Ecology.

General Overviews

The works in this section provide important pieces of the big picture, with respect to humans’ dramatic manipulation of the global nitrogen (N) cycle. Vitousek, et al. 1997 describes the major human activities—fossil fuel combustion, fertilizer N use, land use change, and invasive species introductions—that have changed the way N cycles in air, land, and water systems, while Canfield, et al. 2010 gives an evolutionary and microbial perspective. Also included are primary examples of human impacts on the N cycle; Driscoll, et al. 2001 discusses the generation of acid rain from fossil fuel combustion and the consequences for receiving forest and aquatic ecosystems. The overviews Galloway, et al. 2004 and Galloway, et al. 2008 focus on global estimates of N fluxes and provide recommendations for the management of reactive N (e.g., ammonium and nitrate), acknowledging that it is a problem of “too much” in industrialized regions of the world and “too little” in others, such as parts of the African continent. This section also includes papers on the manipulation of N in rapidly developing countries, including an analysis of China (Cui, et al. 2013), and the potential links between human manipulation of the N cycle and public health (Townsend, et al. 2003). Finally, Fowler, et al. 2013 provides information on current understanding of the global N cycle. Together, these works are meant to give readers an introduction to the vast influence that humans are having over a biogeochemical cycle fundamental to sustaining life on Earth, and to provide context for exploring particular parts of this story in greater detail.

  • Canfield, D. E., A. N. Glazer, and P. G. Falkowski. 2010. The evolution and future of Earth’s nitrogen cycle. Science 330.6001: 192–196.

    DOI: 10.1126/science.1186120Save Citation »Export Citation » Share Citation »

    A discussion of human manipulation of the global N cycle from the perspective of microbial ecology and Earth’s evolution.

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  • Cui, S., Y. Shi, P. M. Groffman, W. H. Schlesinger, and Y.-G. Zhu. 2013. Centennial-scale analysis of the creation and fate of reactive nitrogen in China (1910–2010). Proceedings of the National Academy of Sciences 110.52: 20882–20887.

    DOI: 10.1073/pnas.1012878108Save Citation »Export Citation » Share Citation »

    Manipulation of the N cycle and negative consequences of these activities is currently a major concern in rapidly developing China. This article provides an overview of the major issues for the future.

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  • Driscoll, C. T., G. B. Lawrence, A. J. Bulger, et al. 2001. Acidic deposition in the Northeastern United States: Sources and inputs, ecosystem effects, and management strategies. BioScience 51.3: 180–198.

    DOI: 10.1641/0006-3568Save Citation »Export Citation » Share Citation »

    An overview of how anthropogenic emissions of N (and sulfur, S) form acid rain, which has negative consequences for receiving terrestrial and aquatic ecosystems. Acid rain and its ecosystem effects have been widely studied and publicized in the northeastern United States and Europe since the mid-20th century.

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  • Fowler, D., J. A. Pyle, J. A. Raven, and M. A. Sutton. 2013. The global nitrogen cycle in the twenty-first century: Introduction. Philosophical Transactions of the Royal Society 368.1621.

    DOI: 10.1098/rstb.2013.0165Save Citation »Export Citation » Share Citation »

    An introduction to a suite of papers updating current understanding of the global N cycle, following a meeting at the Royal Society on 4–6 December 2011.

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  • Galloway, J. N., F. J. Dentener, D. G. Capone, et al. 2004. Nitrogen cycles: Past, present, and future. Biogeochemistry 70:153–226.

    DOI: 10.1007/s10533-004-0370-0Save Citation »Export Citation » Share Citation »

    This paper synthesizes several datasets to predict the global N budget in 2050, and highlights human activities that are most impacting the N cycle.

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  • Galloway, J. N., A. R. Townsend, J. W. Erisman, et al. 2008. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320.5878: 889–892.

    DOI: 10.1126/science.1136674Save Citation »Export Citation » Share Citation »

    Updates current understanding of reactive N creation and impacts, including the points: reducing reactive N creation is difficult, but not impossible, and attention to areas with large populations but insufficient N is important, so that they might develop ways to increase food production while minimizing negative impacts on ecosystems.

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  • Townsend, A. R., R. W. Howarth, F. A. Bazzaz, et al. 2003. Human health effects of a changing global nitrogen cycle. Frontiers in Ecology and the Environment 1:240–246.

    DOI: 10.1890/1540-9295(2003)001Save Citation »Export Citation » Share Citation »

    This paper outlines the potential human health risk of an altered global N cycle. Discusses how air- and water-borne N are linked to respiratory conditions, heart disease, cancers, and potentially the spread of vector-borne diseases.

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  • Vitousek, P. M., J. D. Aber, R. W. Howarth, et al. 1997. Human alteration of the global nitrogen cycle: Sources and consequences. Ecological Applications 7:737–750.

    DOI: 10.1890/1051-0761(1997)007Save Citation »Export Citation » Share Citation »

    This is now considered a classic work documenting the primary evidence for human manipulation of the global N cycle.

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A Selection of Relevant Texts and Meetings

There are several scientific meetings, journals, and other texts that pertain to the topic of human manipulation of the N cycle. The American Geophysical Union (AGU) meeting has a growing Biogeosciences section, and, annually, there are several days of presentations and discussion forums that are relevant to this topic and cut across the disciplines of ecology, biogeochemistry, atmospheric sciences, remote sensing, and ocean sciences. The annual Ecological Society of America (ESA) meetings have a strong ecosystem biogeochemistry contingency and often have sessions that include presentations extending beyond the science to societal and economic implications. Other smaller meetings include the Gordon Research Conference on Catchment Science: Interactions of Hydrology, Biology, and Geochemistry, and BIOGEOMON. For scientific journals, readers should see the compilation by W. H. Schlesinger in Biogeochemistry in Oxford Bibliographies in Ecology. These selections are relevant to human dimensions of the N cycle and to biogeochemistry, more broadly. Select texts that would be suitable for upper-level undergraduates and graduate students to learn about altered N cycling include Chapin, et al. 2011 and Schlesinger and Bernhardt 2013 for terrestrial ecosystems and Sarmiento and Gruber 2006 for the oceans. Other resources include Howarth 2011, a SCOPE volume on the N cycle in the North Atlantic Ocean that is a great resource for understanding one of the most impacted areas of the globe, and Townsend 1999, a compilation of articles focused on N cycling in temperate and tropical regions. Likens 2013 provides an understanding of the biogeochemistry of N and other constituents using long-term data from manipulative experiments at the Hubbard Brook Experimental Forest. Finally, Paul 2014 provides an introduction to the organisms and processes underlying the N cycle, and Mosier, et al. 2004 describes how agricultural practices and intensification affect N cycling.

  • Chapin, F. S., P. A. Matson, P. M. Vitousek, and M. C. Chapin. 2011. Principles of terrestrial ecosystem ecology. 2d ed. New York: Springer.

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    Provides sections on biogeochemical cycling, including anthropogenic effects, as well as links to ecological theory. This resource is appropriate for upper-level undergraduates and graduate students.

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  • Howarth, R. W. 2011. Nitrogen cycling in the North Atlantic Ocean and its watersheds: Report of the International SCOPE Nitrogen Project. London: Kluwer Academic.

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    A collection of articles focused on one of the regions most impacted by human influence over the N cycle.

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  • Likens, G. E. 2013. Biogeochemistry of a forested ecosystem. 3d ed. New York: Springer.

    DOI: 10.1007/978-1-4614-7810-2Save Citation »Export Citation » Share Citation »

    The impacts of anthropogenic activities on biogeochemical patterns and processes as shown through long-term datasets collected at the Hubbard Brook Experimental Forest. A great testament to the power of long-term datasets.

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  • Mosier, A. R., J. K. Syers, and J. R. Freney. 2004. Agriculture and the nitrogen cycle: Assessing the impacts of fertilizer use on food production and the environment (SCOPE). 2d ed. Washington, DC: Island Press.

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    An important compilation of articles covering one of the greatest pressures on the N cycle today.

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  • Paul, E. 2014. Soil microbiology, ecology, and biochemistry. 4th ed. Oxford: Academic Press.

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    A great resource on soils, their function, and microorganisms. Useful for understanding the belowground controls on N cycling.

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  • Sarmiento, J. L., and N. Gruber. 2006. Ocean biogeochemical dynamics. Princeton, NJ: Princeton Univ. Press.

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    A useful resource on ocean biogeochemistry for upper-level undergraduates and graduate students.

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  • Schlesinger, W. H., and E. S. Bernhardt. 2013. Biogeochemistry: An analysis of global change. 3d ed. Oxford: Academic Press.

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    A very detailed resource on the topic of altered biogeochemical cycles; a great resource for graduate students.

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  • Townsend, A. R. 1999. New perspectives on nitrogen cycling in the temperate and tropical Americas: Report of the International SCOPE Nitrogen Project. Dordrecht, The Netherlands, and Boston: Kluwer Academic.

    DOI: 10.1007/978-94-011-4645-6Save Citation »Export Citation » Share Citation »

    While estimates of N budgets for many of the articles in this anthology have since been updated, this is a great starting place for readers interested in understanding N manipulation in a variety of ecosystems, and at the global scale. It includes articles by many of the experts on the topic.

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Terrestrial Ecosystems

Nitrogen is a vital and often limiting nutrient in terrestrial ecosystems. Since the 1900s, increases in anthropogenic N deposition to the biosphere have increased the rates of N cycling in soils, changed plant species composition and growth rates, increased fluxes of gaseous N to the atmosphere and dissolved N to downgradient aquatic systems. Beginning in the 1950s, small watershed studies in northeastern US forests first documented the effects of forest management on biogeochemical cycling and hydrology. Likens, et al. 1970 (cited under Human-Dominated Ecosystems) describes this early research. During the 1960s and 1970s, studies investigating how high N deposition affects terrestrial ecosystems began. These studies demonstrated that byproducts of fossil fuel production—gaseous forms of N and sulfur (S)—could be transported long distances in the atmosphere and rain down as strong acids on remote forested ecosystems, as described by Likens, et al. 1972. In terrestrial and aquatic ecosystems, the effects of “acid rain” included changes to soil and surface water pH, release of metals from soils into surface waters at levels toxic to fish and other wildlife, changes to soil biogeochemical processes, and tree mortality (see Driscoll, et al. 2001, cited under General Overviews). Simultaneous to the start of what would become long-term studies of ecosystem decline and then recovery in response to the Clean Air Act and its amendments, other investigators identified the fundamental role that N plays in controlling net primary productivity. For an accessible overview of this relationship, readers should see Chapin, et al. 2011. In addition, investigators developed theories of N saturation in forested ecosystems, such as that articulated by Aber, et al. 1998. Later efforts included large-scale manipulative experiments to understand the effects on N enrichment in a variety of forested ecosystems; included in this section are descriptions of these experiments by Magill, et al. 2004 (for the Harvard Forest Long-term Ecological Research site), Gundersen, et al. 1998, and Wright and Rasmussen 1998 (for the NITRogen saturation EXperiments, NITREX, and the EXperimental MANipulation of Forest Ecosystems in Europe, EXMAN, projects). Similarly, Wedin and Tilman 1996 describes a well-known study of N enrichment in grassland ecosystems, and Matson, et al. 2002 provides a global perspective on the responses of terrestrial ecosystems to high N loading.

  • Aber, J. A., W. McDowell, K. Nadelhoffer, et al. 1998. Nitrogen saturation in temperate forest ecosystems. Bioscience 48.11: 921–934.

    DOI: 10.2307/1313296Save Citation »Export Citation » Share Citation »

    This paper covers control of N over ecosystem productivity and soil carbon sequestration, as well as the potential consequences of high atmospheric N deposition on forested ecosystems.

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  • Chapin, F. S., P. A. Matson, P. M. Vitousek, and M. C. Chapin. 2011. Principles of terrestrial ecosystem ecology. 2d ed. New York: Springer.

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    This is a very good general textbook on ecosystem ecology, appropriate for upper-level undergraduates and graduate students. It contains sections that generally describe human manipulation of the global N cycle and would be of interest to those wanting an introduction to the topic in terrestrial ecosystems.

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  • Gundersen, P., B. A. Emmett, O. J. Kjønaas, C. J. Koopmans, and A. Tietema. 1998. Impact of nitrogen deposition on nitrogen cycling in forests: A synthesis of NITREX data. Forest Ecology and Management 101.1–3: 37–55.

    DOI: 10.1016/S0378-1127(97)00124-2Save Citation »Export Citation » Share Citation »

    Analysis of data from the NITRogen saturation EXperiments (NITREX), a well-known, multisite, N addition experiment in European coniferous forests.

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  • Likens, G. E., F. H. Bormann, and N. M. Johnson. 1972. Acid rain. Environment: Science and Policy for Sustainable Development 14.2: 33–40.

    DOI: 10.1080/00139157.1972.9933001Save Citation »Export Citation » Share Citation »

    An early explanation of how N oxides from combustion are transported many kilometers from their sources and deposited to terrestrial and aquatic systems.

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  • Magill, A. H., J. D. Aber, W. S. Currie, et al. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. Forest Ecology and Management 196.1: 7–28.

    DOI: 10.1016/j.foreco.2004.03.033Save Citation »Export Citation » Share Citation »

    Results of a long-term study quantifying changes to forest N cycling under elevated N deposition. Data link high N inputs to changes in ecosystem function (e.g., high losses of dissolved inorganic N from soils, and elevated foliar and root N concentrations) and structure (e.g., mortality of red maple trees).

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  • Matson, P. A., K. A. Lohse, and S. J. Hall. 2002. The globalization of nitrogen deposition: Consequences for terrestrial ecosystems. AMBIO 31.2: 113–119.

    DOI: 10.1579/0044-7447-31.2.113Save Citation »Export Citation » Share Citation »

    This paper discusses the potential fates and consequences of anthropogenic N deposition in different terrestrial ecosystems, making the point that the response of terrestrial ecosystems will differ based on a number of ecological and state factors.

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  • Wedin, D. A., and D. Tilman. 1996. Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–1723.

    DOI: 10.1126/science.274.5293.1720Save Citation »Export Citation » Share Citation »

    A well-known experiment in species community shifts and changes in soil N cycling as a result of high N applications.

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  • Wright, R. F., and L. Rasmussen. 1998. Introduction to the NITREX and EXMAN projects. In Special Issue: The Whole Ecosystem Experiments of the NITREX and EXMAN projects. Edited by R. F. Wright and L. Rasmussen. Forest Ecology and Management 101.1–3: 1–7.

    DOI: 10.1016/S0378-1127(97)00120-5Save Citation »Export Citation » Share Citation »

    Introduction to a special journal issue describing data from two well-known, important European studies: the NITRogen saturation EXperiments (NITREX) and EXperimental MANipulation of Forest Ecosystems in Europe (EXMAN) projects. Other papers within this issue describe focused studies of N pattern and process conducted within the NITREX and EXMAN sites.

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Inland Rivers

This collection of works provides a starting place for understanding how N enrichment of rivers and streams affects their ecological function. Beginning with the classic paper Gorham 1961, the connections among human activities, atmospheric deposition, and surface water chemistry are described. Such early studies identified that a major concern in surface waters is stimulation of excess algal growth (eutrophication) by limiting nutrients made available at high concentrations from anthropogenic deposition and runoff to biota. While phosphorus (P) was thought to be the primary limiting nutrient in freshwater ecosystems, many studies, including those discussed in the review Elser, et al. 1990, have shown that N can also be limiting, and that experimental additions of both nutrients actually stimulate the greatest biological response. With an understanding of the sources and ecosystem processes contributing to stream and river N loads, researchers have been motivated to inform how to decrease negative consequences. Craig, et al. 2008 presents strategies for restoring streams degraded by high N loads, and Mitsch, et al. 2001 takes on the distributed problem of optimizing strategies for N removal within the Mississippi River Basin to reduce development of the Gulf of Mexico Dead Zone. A large body of research has identified the significant role that riparian zones play in processing N and other nutrients within landscapes, affecting the amount of N transferred from terrestrial to aquatic ecosystems. Hanson, et al. 1994 presents the potential fates of N within riparian zones. Finally, to provide readers with perspective on riverine N transport at larger scales, the works Boyer, et al. 2002 and van Breemen, et al. 2002 provide assessments of N inputs and losses for northeastern US watersheds, which are some of the most impacted by anthropogenic N deposition in the world, and Green, et al. 2004 provides global estimates of riverine N loads, contrasting current and pre-industrialization estimates.

  • Boyer, E. W., C. L. Goodale, N. A. Jaworski, and R. W. Horwath. 2002. Anthropogenic nitrogen sources and relationships to riverine nitrogen export in the northeastern USA. In The nitrogen cycle at regional to global scales. Edited by Elizabeth W. Boyer and Robert W. Howarth, 137–169. New York: Springer.

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    Input and output budgets of sixteen major catchments across a climate gradient in the northeastern United States.

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  • Craig, L. S., M. A. Palmer, D. C. Richardson, et al. 2008. Stream restoration strategies for reducing river nitrogen loads. Frontiers in Ecology and the Environment 6:529–538.

    DOI: 10.1890/070080Save Citation »Export Citation » Share Citation »

    Outlines approaches and priorities for stream restoration that factor N loading mitigation into the effort. The authors consider balancing other major nutrient cycles and optimizing stream physical and ecological characteristics to remove N.

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  • Elser, J. J., E. R. Marzolf, and C. R. Goldman. 1990. Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: A review and critique of experimental enrichments. Canadian Journal of Fisheries and Aquatic Sciences 47.7: 1468–1477.

    DOI: 10.1139/f90-165Save Citation »Export Citation » Share Citation »

    A review of nutrient addition (N, P, and N plus P) experiments in lakes. Demonstrates that not only P, but also N, can limit growth in freshwater systems. Experiments in which these nutrients are both elevated (i.e., N plus P fertilization) showed the greatest algal growth (i.e., eutrophication).

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  • Gorham, E. 1961. Factors influencing supply of major ions to inland waters, with special reference to the atmosphere. Geological Society of America Bulletin 77.6: 795–840.

    DOI: 10.1130/0016-7606(1961)72Save Citation »Export Citation » Share Citation »

    A classic paper that describes the multiple factors influencing surface water chemistry, and identifies the important links among human activities, atmospheric deposition, and surface water chemistry.

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  • Green, P. A., C. J. Vörösmarty, M. Meybeck, J. N. Galloway, B. J. Peterson, and E. W. Boyer. 2004. Pre-industrial and contemporary fluxes of nitrogen through rivers: a global assessment based on typology. Biogeochemistry 68:71–105.

    DOI: 10.1023/B:BIOG.0000025742.82155.92Save Citation »Export Citation » Share Citation »

    A modeling study that synthesizes estimates of global reactive N deposition to land, and calculates subsequent N export via riverine fluxes to the oceans. The authors report a doubling of river N fluxes between preindustrial and present time periods.

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  • Hanson, G. C., P. M. Groffman, and A. J. Gold. 1994. Symptoms of nitrogen saturation in a riparian wetland. Ecological Applications 4.4: 750–756.

    DOI: 10.2307/1942005Save Citation »Export Citation » Share Citation »

    A process-based study showing different pathways of N transformations within the riparian zone of a stream (i.e., terrestrial-aquatic interface). Provides a good discussion of the potential fates of high N loads to these important areas of the landscape.

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  • Mitsch, W. J., J. W. Day Jr., J. W. Gilliam, et al. 2001. Reducing nitrogen loading to the Gulf of Mexico from the Mississippi River Basin: Strategies to counter a persistent ecological problem. BioScience 51:373–388.

    DOI: 10.1641/0006-3568(2001)051Save Citation »Export Citation » Share Citation »

    This article addresses how within watershed processing of N could reduce export to sensitive coastal ecosystems, specifically, the Gulf of Mexico, where persistent eutrophication led to the development of the Dead Zone.

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  • van Breemen, N., E. W. Boyer, C. L. Goodale, et al. 2002. Where did all the nitrogen go? Fate of nitrogen inputs to large watersheds in the northeastern U.S.A. Biogeochemistry 57.58: 267–293.

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    Nitrogen budgets for sixteen large watersheds in the northeastern United States that show primary storage and flows. The authors report that the majority of N is lost in gaseous forms (51 percent), followed by riverine N export (20 percent). These losses can have detrimental effects on adjacent atmospheric and aquatic ecosystems.

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Coastal Ecosystems

High N loads transported to N-limited coastal environments (e.g., estuaries, deltas, and other near-shore ecosystems) can stimulate high rates of primary production, leading to consumption of dissolved oxygen and, over time, development of hypoxic or dead zones. Rabalais and Turner 2001 provides a well-known, well-studied example of high N loads and associated negative consequences in the Gulf of Mexico, which has received years of N loading from intensive agriculture in the Mississippi River Basin. Ahrens, et al. 2008 and Beman, et al. 2005 provide another example of the impacts of N loading to coastal zones from fertilizer use in the Yaqui Valley, Mexico, home of the Green Revolution. Within estuarine systems, N enrichment can alter food webs, as shown by McClelland, et al. 1997, which followed the fate of N using stable isotope approaches and demonstrated the secondary effects that N runoff can have on ecological systems. Finally, observed and modeled estimates of river N export to coastal zones by Howarth, et al. 1996 for the North Atlantic (US) and described by Seitzinger, et al. 2005 for the world, illustrate the links between terrestrial and marine systems. Together, these works provide the reader with a journey from early identification of the issues associated with high N loads from terrestrial to coastal ecosystems, to a processed-based understanding of the consequences at regional to global scales.

  • Ahrens, T. D., J. M. Beman, J. A. Harrison, P. K. Jewett, and P. A. Matson. 2008. A synthesis of nitrogen transformations and transfers from land to sea in the Yaqui Valley agricultural region of northwest Mexico. Water Resources Research 44.7.

    DOI: 10.1029/2007WR006661Save Citation »Export Citation » Share Citation »

    A synthesis of data from a ten-year study following the fates and transport of N fertilizers in the intensive agricultural region of the Yaqui Valley, Mexico (home of “The Green Revolution”).

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  • Beman, J. M., K. R. Arrigo, and P. A. Matson. 2005. Agricultural runoff fuels large phytoplankton blooms in the vulnerable areas of the ocean. Nature 434:211–214.

    DOI: 10.1038/nature03370Save Citation »Export Citation » Share Citation »

    Using SeaWiFS imagery, the authors show increases in chlorophyll a in the Gulf of California following irrigation and fertilizer use in the major agricultural region of the Yaqui Valley, Mexico. This article demonstrates a link between management of N and water on land, and biological activity in N-limited coastal areas.

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  • Howarth, R. W., G. Billen, D. Swaney, et al. 1996. Regional nitrogen budgets and riverine N and P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences. Biogeochemistry 35:75–139.

    DOI: 10.1007/BF02179825Save Citation »Export Citation » Share Citation »

    A good synthesis of data for the North Atlantic region.

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  • McClelland, J. W., I. Valiela, and R. H. Michener. 1997. Nitrogen-stable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds. Limnology and Oceanography 42.5: 930–937.

    DOI: 10.4319/lo.1997.42.5.0930Save Citation »Export Citation » Share Citation »

    A valuable illustration of how land use—urbanization, in this example—influences the ecology and N cycling of receiving aquatic ecosystems.

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  • Rabalais, N. N., and R. E. Turner, eds. 2001. Hypoxia in the Northern Gulf of Mexico: Description, causes, and change. Washington, DC: American Geophysical Union.

    DOI: 10.1029/CE058Save Citation »Export Citation » Share Citation »

    The Gulf of Mexico Dead Zone is a well known, well-studied example of the effects of high N loads to coastal ecosystems. This book provides an overview of the factors contributing to the development of hypoxia, as well as the ecological consequences.

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  • Seitzinger, S. P., J. A. Harrison, E. Dumont, A. H. W. Beusen, and A. F. Bouwman. 2005. Sources and delivery of carbon, nitrogen, and phosphorus to the coastal zone: An overview of Global Nutrient Export from Watersheds (NEWS) models and their application. Global Biogeochemical Cycles 19.4.

    DOI: 10.1029/2005GB002606Save Citation »Export Citation » Share Citation »

    Simulations of C, N, and P export from 5761 watersheds globally. Incorporates the drivers of land use, nutrient inputs, and hydrology, and considers how they will affect the forms, amounts, and ratios of nutrients exported from land to sea.

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The Open Ocean

Anthropogenic N sources are not only a concern over land, but also within marine systems. Nitrogen enters the ocean as export from terrestrial ecosystems (delivered via runoff) or direct atmospheric deposition. In the open ocean, both physical and biological controls contribute to the residence time and fate of N. Excess N inputs can increase rates of net primary productivity, thereby increasing the amount of carbon and other nutrients that are cycled and recycled within the water column. Net primary productivity is a major control on N turnover in surface waters, while the sinking of dead material from surface waters through the thermocline—known as “the biological pump”—is a source of N to the deep ocean. Physical controls (e.g., transport, eddy circulation dynamics, and upwelling) also influence the fate and distribution of N in the oceans. Over time, the loss of N from surface waters must be balanced by new inputs and/or upwelling from the deep ocean. For general background on the cycling of N and other elements in the ocean, readers should consult Sarmiento and Gruber 2006. For a more detailed perspective, Karl, et al. 2002 and Zehr and Ward 2002 describe changes to N cycling at the scale of microorganisms. Duce, et al. 2008 and Paerl 1985 use observations to examine the role of atmospheric anthropogenic N deposition in changing oceanic N cycling, while Krishnamurthy, et al. 2009 communicates changes to primary productivity using an oceanic model. Finally, Deutsch, et al. 2007 provides a good summary on the N balance of the oceans, and Michaels, et al. 1996 reports a synthesis of data for N sources and stocks in the Atlantic Ocean, which is the ocean most strongly influenced by N export from industrialized nations.

  • Deutsch, C., J. L. Sarmiento, D. M. Sigman, N. Gruber, and J. P. Dunne. 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445:163–167.

    DOI: 10.1038/nature05392Save Citation »Export Citation » Share Citation »

    Provides a good summary of the N balance in the oceans.

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  • Duce, R. A., J. LaRoche, K. Altieri, et al. 2008. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320.5878: 893–897.

    DOI: 10.1126/science.1150369Save Citation »Export Citation » Share Citation »

    Details human impacts on N cycling in the ocean.

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  • Karl, D., A. Michaels, B. Bergman, et al. 2002. Dinitrogen fixation in the world’s oceans. In The nitrogen cycle at regional to global scales. Edited by Elizabeth W. Boyer and Robert W. Howarth, 47–98. New York: Springer.

    DOI: 10.1007/978-94-017-3405-9Save Citation »Export Citation » Share Citation »

    An introduction to N cycling processes in the ocean, both background and human-influenced, at the level of microorganisms. This chapter would be accessible to both upper-level undergraduates and graduate students.

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  • Krishnamurthy, A., J. K. Moore, N. Mahowald, et al. 2009. Impacts of increasing anthropogenic soluble iron and nitrogen deposition on ocean biogeochemistry. Global Biogeochemical Cycles 23:GB3016.

    DOI: 10.1029/2008GB003440Save Citation »Export Citation » Share Citation »

    A modeling study that quantifies the effects of high iron (Fe) and inorganic N deposition to the ocean. The investigators showed that combined Fe and N additions yielded the greatest response by primary producers.

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  • Michaels, A. F., D. Olson, J. L. Sarmiento, et al. 1996. Inputs, losses, and transformations of nitrogen and phosphorus in the pelagic North Atlantic Ocean. In Nitrogen cycling in the North Atlantic Ocean and its watersheds. Edited by Robert W. Howarth, 181–226. New York: Springer.

    DOI: 10.1007/978-94-009-1776-7Save Citation »Export Citation » Share Citation »

    Provides data on the sources and stocks of N in the Atlantic Ocean, which receives the largest quantities of allochthonous N due to the influences of nearby industrialized countries.

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  • Paerl, H. W. 1985. Enhancement of marine primary production by nitrogen-enriched acid rain. Nature 315:747–749.

    DOI: 10.1038/315747a0Save Citation »Export Citation » Share Citation »

    This study reports a direct link between atmospheric deposition of N (in acid rain) and stimulation of phytoplankton growth in marine systems.

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  • Sarmiento, J. L., and N. Gruber. 2006. Ocean biogeochemical dynamics. Princeton, NJ: Princeton Univ. Press.

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    An excellent resource detailing the biogeochemistry of N and other elements in the ocean.

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  • Zehr, J. P., and B. B. Ward. 2002. Nitrogen cycling in the ocean: New perspectives on processes and paradigms. Applied and Environmental Microbiology 68.3: 1015–1024.

    DOI: 10.1128/AEM.68.3.1015-1024.2002Save Citation »Export Citation » Share Citation »

    A discussion of how the marine N cycle is influenced by processes occurring at the level of microorganisms, and how technological advances in this area of study will help to provide further insight into how a changing N cycle is impacting the ocean system.

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Human-Dominated Ecosystems

Climate change, land use/land cover change, invasive species, and other drivers exert control over the N cycle at multiple scales. Therefore, it is important to highlight N dynamics in terrestrial ecosystems where people are a major, direct influence on the landscape. This section includes a suite of papers that describe changes to N cycling in ecosystems impacted by invasive species, agricultural systems, regions of deforestation, and urban landscapes. The changes to N cycling that occur as a result of these activities vary, and the effects can be seen locally and/or remotely. Vitousek 1996 describes how invasive species—sometimes introduced by humans—can alter the structure and function of the ecosystems they occupy, thereby changing N and other biogeochemical cycles. Smil 2001 details how croplands involve decisions about management of N fertilizers and irrigation. The impacts of crop management on N cycling can be observed locally, such as by increasing emissions of the greenhouse gas nitrous oxide (N2O) from cultivated soils, as shown by Reay, et al. 2012, and by enriching runoff transported to N-limited coastal zones (see Beman, et al. 2005, cited under Coastal Ecosystems). Livestock production influences N cycling in other ways; it is highly resource-intensive, requiring feed, water, and land, and the animals themselves are major sources of greenhouse gas emissions, as demonstrated by Bouwman, et al. 2011. Likens, et al. 1970 and Robertson and Tiedje 1988 provide early studies on how deforestation changes rates of soil N cycling, as well as transport of N to downgradient aquatic systems, while Collins, et al. 2010 shows that urban environments quickly transport high concentrations of N species in runoff from a variety of sources to downgradient aquatic environments. Finally, Kinzig and Socolow 1994 demonstrates the record of far-reaching human influence on the global N cycle, as captured in ice cores collected in polar regions. This sampling of the relevant research provides an entrée to one of the primary societal challenges we now face with respect to our manipulation of the N cycle: to reverse the harmful consequences of our activities, and to transition to more sustainable practices for the future.

  • Bouwman, L., K. K. Goldewijk, K. W. Van Der Hoek, et al. 2011. Exploring global changes in nitrogen and phosphorus cycles in agriculture induced by livestock production over the 1900–2050 period. Proceedings of the National Academy of Sciences 110.52: 20882–20887.

    DOI: 10.1073/pnas.1012878108Save Citation »Export Citation » Share Citation »

    Explores changes to the global N (and P) budgets based on current data for crop and livestock activities that alter the creation, use, and movement of these constituents.

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  • Collins, K. A., T. J. Lawrence, E. K. Stander, et al. 2010. Opportunities and challenges for managing nitrogen in urban stormwater: A review and synthesis. Ecological Engineering 36.11: 1507–1519.

    DOI: 10.1016/j.ecoleng.2010.03.015Save Citation »Export Citation » Share Citation »

    A review of the issues and concerns with N pollution in water exported from urban watersheds.

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  • Kinzig, A. P., and R. H. Socolow. 1994. Human impacts on the nitrogen cycle. Physics Today 47.11: 24.

    DOI: 10.1063/1.881423Save Citation »Export Citation » Share Citation »

    Reports nitrous oxide (N2O) concentrations from ice cores taken in the Arctic and Antarctic, demonstrating the rapid increase in present-day atmospheric N that was captured in systems thought to be remote and relatively unaltered by human activity.

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  • Likens, G. E., F. H. Bormann, N. M. Johnson, D. W. Fisher, and R. S. Pierce. 1970. Effects of forest cutting and herbicide treatment on nutrient budgets in the Hubbard Brook Watershed-Ecosystem. Ecological Monographs 40:23–47.

    DOI: 10.2307/1942440Save Citation »Export Citation » Share Citation »

    Publication of one of the classic early experiments at a Long-term Ecological Research (LTER) site demonstrating that clear-cutting of forests can change soil N cycling and losses from terrestrial ecosystems.

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  • Reay, D. S., E. A. Davidson, K. A. Smith, et al. 2012. Global agriculture and nitrous oxide emissions. Nature Climate Change 2:410–416.

    DOI: 10.1038/nclimate1458Save Citation »Export Citation » Share Citation »

    Presents the concerns regarding emissions of the greenhouse gas nitrous oxide (N2O) from croplands to the atmosphere, as well as estimates of total emissions from agricultural lands and suggestions for controlling emissions through reducing demand for particular agricultural products.

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  • Robertson, G. P., and J. M. Tiedje. 1988. Deforestation alters denitrification in a lowland tropical rain forest. Nature 336.22: 756–759.

    DOI: 10.1038/336756a0Save Citation »Export Citation » Share Citation »

    Rates of denitrification, a major loss pathway of N from terrestrial and aquatic ecosystems to the atmosphere, are high in primary forest and early successional areas and low in mid-successional areas of the humid tropics.

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  • Smil, V. 2001. Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food production. Cambridge, MA: MIT Press.

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    Describes the industrialization of agriculture and the support of a growing human population through synthesis and commercialization of N fertilizers. Includes discussion of different N fertilizers in crop systems, the dependence of modern society on these amendments, and the unintended consequences for air, land, and water systems.

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  • Vitousek, Peter M. 1996. Biological invasions and ecosystem processes: Towards an integration of population biology and ecosystem studies. In Ecosystem management. Edited by Fred B. Samson and Fritz L. Knopf, 183–191. New York: Springer.

    DOI: 10.1007/978-1-4612-4018-1Save Citation »Export Citation » Share Citation »

    An accessible introduction to the role that species invasions play in altering ecosystem function. This chapter highlights both natural and anthropogenic drivers.

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Interactions of Nitrogen with Climate, Hydrology, and Other Biogeochemical Cycles

The global biogeochemical cycles of C, N, and P are linked to one another; a perturbation in one cycle can stimulate change in another. For example, additions of N to forest soils can influence belowground C sequestration or aboveground biomass accumulation, as demonstrated by Pinder, et al. 2013. The climate system and hydrology, which are also subject to anthropogenic changes, further influence the interactions among biogeochemical cycles. Gruber and Galloway 2008 nicely articulates how the interplay between climate and biogeochemical cycles influences the functioning of the Earth system. Focusing on the continental scale, Baron, et al. 2013 demonstrates how interactions between reactive N and climate have extensive effects on the health of aquatic ecosystems. A specific, regional example of the connections between climate, the N cycle, and surface water chemistry is given by Williams, et al. 1996, which shows that in the Colorado Front Range of the Rocky Mountains (US), high N loads to sensitive alpine ecosystems are directly proportional to the amount of snowfall, which affects the concentrations of nitrate in surface waters during spring snowmelt. Also included in this section are Neff, et al. 2002 and Doney, et al. 2007, which explore the links between anthropogenic N loads and the C balance of soils and the ocean, respectively. Finally, Carpenter, et al. 1998 and Schindler, et al. 2008 attempt to untangle the effects of high N and P inputs to surface water systems, where they can cause eutrophication and a range of other negative ecological consequences. These works illustrate the need for multidisciplinary studies at a range of scales and in a variety of ecosystems to address the far-reaching consequences of humans’ manipulation of the global N cycle.

  • Baron, J. S., E. K. Hall, B. T. Nolan, et al. 2013. The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114:71–92.

    DOI: 10.1007/s10533-012-9788-ySave Citation »Export Citation » Share Citation »

    An updated paper detailing how human manipulation of N and the hydrologic cycle affect aquatic ecosystem function.

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  • Carpenter, S. R., N. F. Caraco, D. L. Correll, R. W. Howarth, A. N. Sharpley, and V. H. Smith. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8:559–568.

    DOI: 10.1890/1051-0761(1998)008Save Citation »Export Citation » Share Citation »

    This is a good review of nonpoint source pollution of surface waters with N and P generated by a variety of human activities. It gives a detailed explanation of the roles that both nutrients play in causing eutrophication and other negative consequences in aquatic ecosystems.

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  • Doney, S. C., N. Mahowald, I. Lima, et al. 2007. Impact of anthropogenic atmospheric nitrogen and sulfur deposition on ocean acidification and the inorganic carbon system. Proceedings of the National Academy of Sciences 104.37: 14580–14585.

    DOI: 10.1073/pnas.0702218104Save Citation »Export Citation » Share Citation »

    Describes the effects of acidic forms of N and S deposition, resulting pH dynamics in surface waters, and the ultimate effects on the C balance of the ocean.

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  • Gruber, N., and J. N. Galloway. 2008. An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296.

    DOI: 10.1038/nature06592Save Citation »Export Citation » Share Citation »

    Discusses how human activities are impacting the links among climate drivers, C, N, and P cycles, and how this will have major consequences for the Earth system.

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  • Neff, J. C., A. R. Townsend, G. Gleixner, S. J. Lehman, J. Turnbull, and W. D. Bowman. 2002. Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917.

    DOI: 10.1038/nature01136Save Citation »Export Citation » Share Citation »

    Evaluates the effect of N fertilization on the decomposition of different C fractions (light and heavy). The investigators show that N additions increase the rates of decomposition for light soil C fractions, and stabilize heavy soil C fractions.

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  • Pinder, R. W., N. D. Bettez, G. B. Bonan, et al. 2013. Impacts of human alteration of the nitrogen cycle in the US on radiative forcing. Biogeochemistry 114.1–3: 25–40.

    DOI: 10.1007/s10533-012-9787-zSave Citation »Export Citation » Share Citation »

    This paper shows how different gaseous forms of N in the atmosphere can affect aerosols, as well as be deposited onto terrestrial ecosystems, influencing C sequestration in biomass and soils.

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  • Schindler, D. W., R. E. Hecky, D. L. Findlay, et al. 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input: Results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences 105.32: 11254–11258.

    DOI: 10.1073/pnas.0805108105Save Citation »Export Citation » Share Citation »

    This synthesis of a well-known, long-term, whole-lake experiment details interactions between the N and P cycles, and concludes that reducing eutrophication of lakes requires management of P inputs, rather than N inputs.

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  • Williams, M. W., J. S. Baron, N. Caine, R. Sommerfeld, and R. Sanford Jr. 1996. Nitrogen saturation in the Rocky Mountains. Environmental Science and Technology 30:640–646.

    DOI: 10.1021/es950383eSave Citation »Export Citation » Share Citation »

    Describes the response of alpine ecosystems to increasingly high N inputs in snowfall.

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Network Science and Data Resources

The major societal problems we face today—How do we feed a growing population? How do we mitigate or adapt to the threats that climate change poses for our planet’s support systems? How do we reverse environmental degradation?—may be addressed by investigators knowing how to take advantage of infrastructure and data resources provided by the growing number of long-term, spatially extensive observatory networks. An observatory network is a suite of research sites with a particular scientific focus that collects, curates, and provides publicly available data. Some are designed using standardized infrastructure and methodology across all sites, such as the National Ecological Observatory Network (NEON), or through principal investigator-driven projects, such as the Long-Term Ecological Research (LTER) sites and Critical Zone Observatories (CZO). The networks have different focuses; for example, CZO sites focus on gathering data to address questions primarily related to geomorphology and hydrology, NEON and LTER are ecologically focused, AmeriFlux gathers biometeorology data, the Global Lake Ecological Observatory Network (GLEON) monitors the response of lakes to global change drivers, and the Nutrient Network (NutNet) is a grassroots effort to make direct comparisons of environment-productivity-diversity relationships across a broad range of grassland sites. More and more, there is recognition by the scientific community that data must be made a public resource, and increasing investment by major funding organizations, such as the National Science Foundation, in developing network science. Graduate students today should be equipped with the skills they will need to take advantage of these resources, and to learn how to leverage them for their own research. These skills include conceptual understanding of major environmental issues and questions, technical ability (e.g., programming, database management, and statistical analysis), and hands-on experience querying, analyzing, and interpreting large datasets through coursework and research. All of the research networks highlighted in this section are collecting biogeochemical data. Some of them are making direct measurements of N cycle components, while others are collecting data on important drivers of the N cycle, and, thus, may be of interest to readers. This selection represents an introduction to some of the large-scale networks now in operation.

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