David Tilman

HUMAN ALTERATION OF THE GLOBAL NITROGEN CYCLE: SOURCES AND CONSEQUENCES

Nitrogen is a key element controlling the species composition, diversity, dynamics, and functioning of many terrestrial, freshwater, and marine ecosystems. Many of the original plant species living in these ecosystems are adapted to, and function optimally in, soils and solutions with low levels of available nitrogen. The growth and dynamics of herbivore populations, and ultimately those of their predators, also are affected by N. Agriculture, combustion of fossil fuels, and other human activities have altered the global cycle of N substantially, generally increasing both the availability and the mobility of N over large regions of Earth. The mobility of N means that while most deliberate applications of N occur locally, their influence spreads regionally and even globally. Moreover, many of the mobile forms of N themselves have environmental consequences. Although most nitrogen inputs serve human needs such as agricultural production, their environmental conse- quences are serious and long term. Based on our review of available scientific evidence, we are certain that human alterations of the nitrogen cycle have: 1) approximately doubled the rate of nitrogen input into the terrestrial nitrogen cycle, with these rates still increasing; 2) increased concentrations of the potent greenhouse gas N 2O globally, and increased concentrations of other oxides of nitrogen that drive the formation of photochemical smog over large regions of Earth; 3) caused losses of soil nutrients, such as calcium and potassium, that are essential for the long-term maintenance of soil fertility; 4) contributed substantially to the acidification of soils, streams, and lakes in several regions; and 5) greatly increased the transfer of nitrogen through rivers to estuaries and coastal oceans. In addition, based on our review of available scientific evidence we are confident that human alterations of the nitrogen cycle have: 6) increased the quantity of organic carbon stored within terrestrial ecosystems; 7) accelerated losses of biological diversity, especially losses of plants adapted to efficient use of nitrogen, and losses of the animals and microorganisms that depend on them; and 8) caused changes in the composition and functioning of estuarine and nearshore ecosystems, and contributed to long-term declines in coastal marine fisheries.

Agricultural sustainability and intensive production practices

A doubling in global food demand projected for the next 50 years poses huge challenges for the sustainability both of food production and of terrestrial and aquatic ecosystems and the services they provide to society. Agriculturalists are the principal managers of global useable lands and will shape, perhaps irreversibly, the surface of the Earth in the coming decades. New incentives and policies for ensuring the sustainability of agriculture and ecosystem services will be crucial if we are to meet the demands of improving yields without compromising environmental integrity or public health.

Land Clearing and the Biofuel Carbon Debt

Increasing energy use, climate change, and carbon dioxide (CO2) emissions from fossil fuels make switching to low-carbon fuels a high priority. Biofuels are a potential low-carbon energy source, but whether biofuels offer carbon savings depends on how they are produced. Converting rainforests, peatlands, savannas, or grasslands to produce food crop–based biofuels in Brazil, Southeast Asia, and the United States creates a “biofuel carbon debt” by releasing 17 to 420 times more CO2 than the annual greenhouse gas (GHG) reductions that these biofuels would provide by displacing fossil fuels. In contrast, biofuels made from waste biomass or from biomass grown on degraded and abandoned agricultural lands planted with perennials incur little or no carbon debt and can offer immediate and sustained GHG advantages.

Solutions for a cultivated planet

Increasing population and consumption are placing unprecedented demands on agriculture and natural resources. Today, approximately a billion people are chronically malnourished while our agricultural systems are concurrently degrading land, water, biodiversity and climate on a global scale. To meet the world’s future food security and sustainability needs, food production must grow substantially while, at the same time, agriculture’s environmental footprint must shrink dramatically. Here we analyse solutions to this dilemma, showing that tremendous progress could be made by halting agricultural expansion, closing ‘yield gaps’ on underperforming lands, increasing cropping efficiency, shifting diets and reducing waste. Together, these strategies could double food production while greatly reducing the environmental impacts of agriculture.

Biodiversity loss and its impact on humanity

The most unique feature of Earth is the existence of life, and the most extraordinary feature of life is its diversity. Approximately 9 million types of plants, animals, protists and fungi inhabit the Earth. So, too, do 7 billion people. Two decades ago, at the first Earth Summit, the vast majority of the world’s nations declared that human actions were dismantling the Earth’s ecosystems, eliminating genes, species and biological traits at an alarming rate. This observation led to the question of how such loss of biological diversity will alter the functioning of ecosystems and their ability to provide society with the goods and services needed to prosper.

Global food demand and the sustainable intensification of agriculture

Global food demand is increasing rapidly, as are the environmental impacts of agricultural expansion. Here, we project global demand for crop production in 2050 and evaluate the environmental impacts of alternative ways that this demand might be met. We find that per capita demand for crops, when measured as caloric or protein content of all crops combined, has been a similarly increasing function of per capita real income since 1960. This relationship forecasts a 100–110% increase in global crop demand from 2005 to 2050. Quantitative assessments show that the environmental impacts of meeting this demand depend on how global agriculture expands. If current trends of greater agricultural intensification in richer nations and greater land clearing (extensification) in poorer nations were to continue, ∼1 billion ha of land would be cleared globally by 2050, with CO2-C equivalent greenhouse gas emissions reaching ∼3 Gt y−1 and N use ∼250 Mt y−1 by then. In contrast, if 2050 crop demand was met by moderate intensification focused on existing croplands of underyielding nations, adaptation and transfer of high-yielding technologies to these croplands, and global technological improvements, our analyses forecast land clearing of only ∼0.2 billion ha, greenhouse gas emissions of ∼1 Gt y−1, and global N use of ∼225 Mt y−1. Efficient management practices could substantially lower nitrogen use. Attainment of high yields on existing croplands of underyielding nations is of great importance if global crop demand is to be met with minimal environmental impacts.

Competition and Biodiversity in Spatially Structured Habitats

All organisms, especially terrestrial plants and other sessile species, interact mainly with their neighbors, but neighborhoods can differ in composition because of dis- persal and mortality. There is increasingly strong evidence that the spatial structure created by these forces profoundly influences the dynamics, composition, and biodiversity of com- munities. Nonspatial models predict that no more consumer species can coexist at equilibrium than there are limiting resources. In contrast, a similar model that includes neighborhood competition and random dispersal among sites predicts stable coexistence of a potentially unlimited number of species on a single resource. Coexistence occurs because species with sufficiently high dispersal rates persist in sites not occupied by superior competitors. Co- existence requires limiting similarity and two-way or three-way interspecific trade-offs among competitive ability, colonization ability, and longevity. This spatial competition hypothesis seems to explain the coexistence of the numerous plant species that compete for a single limiting resource in the grasslands of Cedar Creek Natural History Area. It provides a testable, alternative explanation for other high diversity communities, such as tropical forests. The model can be tested (1) by determining if coexisting species have the requisite trade-offs in colonization, competition, and longevity, (2) by addition of propagules to determine if local species abundances are limited by dispersal, and (3) by comparisons of the effects on biodiversity of high rates of propagule addition for species that differ in competitive ability.

Carbon-negative biofuels from low-input high-diversity grassland biomass.

Biofuels derived from low-input high-diversity (LIHD) mixtures of native grassland perennials can provide more usable energy, greater greenhouse gas reductions, and less agrichemical pollution per hectare than can corn grain ethanol or soybean biodiesel. High-diversity grasslands had increasingly higher bioenergy yields that were 238% greater than monoculture yields after a decade. LIHD biofuels are carbon negative because net ecosystem carbon dioxide sequestration (4.4 megagram hectare–1 year–1 of carbon dioxide in soil and roots) exceeds fossil carbon dioxide release during biofuel production (0.32 megagram hectare–1 year–1). Moreover, LIHD biofuels can be produced on agriculturally degraded lands and thus need to neither displace food production nor cause loss of biodiversity via habitat destruction.

Challenges in the quest for keystones

Mary E. Power is a professor in the Department of Integrative Biology, University of California, Berkeley, CA 94720. David Tilman is a professor in the Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108. James A. Estes is a wildlife biologist in the National Biological Service, Institute of Marine Science, University of California, Santa Cruz, CA 95064. Bruce A. Menge is a professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. William J. Bond is a professor doctor in the Department of Botany, University of Cape Town, Rondebosch 7700 South Africa. L. Scott Mills is an assistant professor in the Wildlife Biology Program, School of Forestry, University of Montana, Missoula, MT 59812. Gretchen Daily is Bing Interdisciplinary Research Scientist, Department of Biological Science, Stanford University, Stanford, CA 94305. Juan Carlos Castilla is a full professor and marine biology head in Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile. Jane Lubchenco is a distinguished professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. Robert T. Paine is a professor in the Department of Zoology, NJ-15, University of Washington, Seattle, WA 98195. ? 1996 American Institute of Biological Sciences. A keystone species is

Biodiversity: Population Versus Ecosystem Stability

The relationships between biodiversity and stability were determined for both population and ecosystem traits in a long-term study of 207 grassland plots. Results demonstrate that biodiversity stabilizes community and ecosystem processes, but not pop- ulation processes. Specifically, year-to-year variability in total aboveground plant com- munity biomass was significantly lower in plots with greater plant species richness both for the entire 11-yr period and for the nine non-drought years. The change in total plant community biomass from before the drought to the peak of the drought was also highly dependent on species richness. For all three measures of total community biomass stability, multiple regressions that controlled for covariates showed similar significant relationships between plant diversity and stability. In contrast, year-to-year variability in species abundances was not stabilized by plant species richness for either all years or non-drought years. This difference between species vs. community biomass likely results from interspecific competition. When climatic vari- ations harm some species, unharmed competitors increase. Such compensatory increases stabilize total community biomass, but cause species abundances to be more variable. These results support both the predictions of Robert May concerning the effects of diversity on population stability and the diversity-stability hypothesis as applied to community and ecosystem processes, thus helping to reconcile a long-standing dispute.