Colloquium on Plants and Population: Is There Time? 0309064279, 9780309064279

Table of contents :
COLLOQUIUM ON PLANTS AND POPULATION: IS THERE TIME?
Plants and Population: is there time?
Contents
Plants and population: Is there time?
HISTORICAL BACKGROUND
DEMOGRAPHIC SITUATION AND PROSPECT: THE CHALLENGE
COLLOQUIUM GOALS AND STRUCTURE
INSIGHTS FROM THE COLLOQUIUM
CONCLUDING PERSPECTIVE
World food and agriculture: Outlook for the medium and longer term
KEY HISTORICAL DEVELOPMENTS
WORLD PRODUCTION AND FOOD INSECURITY: AN UNCERTAIN LINK.
FUTURE PROSPECTS
CONCLUSIONS
The growth of demand will limit output growth for food over the next quarter century
Global and local implications of biotechnology and climate change for future food supplies
I. INTRODUCTION
II. THE IFPRI–IMPACT MODEL
III. SPECIFYING THE NONPRICE SUPPLY (AREA AND YIELD) TERMS
IV. POLICY SCENARIOS
V. POLICY SIMULATIONS
VI. POLICY IMPLICATIONS
APPENDIX: THE IFPRI–IMPACT MODEL BASE CASE
World food trends and prospects to 2025
CEREAL PRODUCTION TRENDS
THE FUTURE: CEREAL DEMAND AND SUPPLY
CONCLUSION
Plant genetic resources: What can they contribute toward increased crop productivity?
THE ROLE OF THE CONSULTIVE GROUP ON INTERNATIONAL AGRICULTURAL RESEARCH (CGIAR) IN PRESERVING GENETIC RESOURCES
CONTRIBUTIONS OF WHEAT GENETIC RESOURCES
USE OF GENETIC RESOURCES IN MAIZE IMPROVEMENT
INTELLECTUAL PROPERTY RIGHTS ISSUES RELATED TO THE UTILIZATION OF GENETIC RESOURCES
MOLECULAR APPROACHES TO UTILIZATION OF GENETIC RESOURCES
GENETIC RESOURCES: WHAT ARE THE POTENTIAL IMPACTS?
Ecological approaches and the development of "truly integrated" pest management
INTEGRATING BIOLOGICAL CONTROL AND HOST PLANT RESISTANCE FOR CONTROL OF INSECT PESTS
ECOLOGY OF HOST–PATHOGEN INTERACTIONS AND MICROBIAL PEST CONTROL
CONCLUSIONS
Ecological intensification of cereal production systems: Yield potential, soil quality, and precision agriculture
THE NEED FOR ECOLOGICAL INTENSIFICATION
INTENSIFICATION IN FAVORABLE AND UNFAVORABLE ENVIRONMENTS
YIELD POTENTIAL
SOIL QUALITY
PRECISION AGRICULTURE
CONCLUSIONS
The transition to agricultural sustainability
SUSTAINABILITY SCENARIOS
SCIENTIFIC AND TECHNICAL CONSTRAINTS C
RESOURCE AND ENVIRONMENTAL CONSTRAINTS
Biotechnology: Enhancing human nutrition in developing and developed worlds
AGRONOMIC TRAITS
DIFFERENTIATED CROPS
PLANTS AS FACTORIES
Use of plant roots for phytoremediation and molecular farming
CONCLUSIONS
Transgenic plants for tropical regions: Some considerations about their development and their transfer to the small farmer
From pre-Hispanic to future conservation alternatives: Lessons from Mexico
Gardenification of tropical conserved wildlands: Multitasking, multicropping, and multiusers
THE WILDLAND GARDEN
THE WILDLAND YELLOW PAGES
A TALE OF TWO FREEZERS
BIODIVERSITY PROSPECTING
"ENVIRONMENTAL SERVICES CONTRACTS" BETWEEN THE WILDLAND GARDEN AND SOCIETY
BE POSITIVE
APPENDIX I
APPENDIX II
Global environmental impacts of agricultural expansion: The need for sustainable and efficient practices
THE ECOLOGY OF DOUBLING CROP PRODUCTION
ECOLOGICAL IMPACTS OF DOUBLING GLOBAL FOOD PRODUCTION
AGRICULTURE AND THE LOSS OF ECOSYSTEM SERVICES
MORE OF THE SAME WILL NOT WORK
ECOLOGICAL INSIGHTS INTO AGRICULTURAL IMPACTS AND SUSTAINABILITY
CONCLUSIONS
Nitrogen management and the future of food: Lessons from the management of energy and carbon
HOW THE NITROGEN CYCLE WORKS AND HOW IT IS BEING DISRUPTED
WHY THE INCREASE IN STOCKS OF FIXED NITROGEN IS TROUBLESOME
LESSONS FROM CARBON AND ENERGY FOR NITROGEN AND FOOD
CONCLUSIONS

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COLLOQUIUM ON PLANTS AND POPULATION: IS THERE TIME?

NATIONAL ACADEMY OF SCIENCES WASHINGTON, D.C.

1999

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NATIONAL ACADEMY OF SCIENCES Colloquium Series In 1991, the National Academy of Sciences inaugurated a series of scientific colloquia, five or six of which are scheduled each year under the guidance of the NAS Council’s Committee on Scientific Programs. Each colloquium addresses a scientific topic of broad and topical interest, cutting across two or more of the traditional disciplines. Typically two days long, colloquia are international in scope and bring together leading scientists in the field. Papers from colloquia are published in the Proceedings of the National Academy of Sciences (PNAS).

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PLANTS AND POPULATION: IS THERE TIME?

iii

Plants and Population: is there time?

A Colloquium sponsored by the National Academy of Sciences December 5–6, 1998 PROGRAM Saturday, Dec 5, 1998 Session I: Demographic and economic projections of food demand and supply. Session Chair: Joel Cohen, The Rockefeller University World food & agriculture: the outlook for the medium & longer term. Nikos Alexandratos, Food and Agriculture Organization of the United Nations The growth of demand will limit output growth for food over the next quarter century. D. Gale Johnson, University of Chicago Global and local implications of biotechnology and climate change for future food supplies. Robert Evenson, Yale University World food trends and prospects to 2020. Tim Dyson, London School of Economics Panelists: Dennis Ahlburg, University of Minnesota; Kenneth Arrow, Stanford University; Bernard Gilland, Espergaerde, Denmark; Vaclav Smil, University of Manitoba Saturday, Dec 5, 1998 2:00–5:00 Session II: Limits on agriculture: land, water, energy and biological resources. Chair: Michael Clegg, University of California, Riverside Plant genetic resources: what can they contribute towards increased crop productivity? David Hoisington, Centro Internacional de Mejoramiento de Maiz y Trigo, Int. Ecological approaches and the development of ‘truly’ integrated pest management. Matthew Thomas, Centre for Population Biology, Imperial College Ecological intensification of cereal production systems: the challenge of increasing crop yield potential and precision agriculture. Kenneth Cassman, University of Nebraska The transition to agricultural sustainability. Vernon Ruttan, University of Minnesota Panelists: Gretchen Daily, Stanford University; William Murdoch, University of California, Santa Barbara; Billie Lee Turner, Clark University; Catherine Woteki, United States Department of Agriculture After Dinner Speaker: Ismail Serageldin, World Bank, Plants and Population: is there time?

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PLANTS AND POPULATION: IS THERE TIME?

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Sunday, Dec 6, 1998 Session III: Plant and other biotechnologies. Chair: Nina Fedoroff, The Pennsylvania State University Biotechnology: enhancing human nutrition in developing and developed worlds. Ganesh Kishore, Monsanto Use of plant roots for environmental remediation and biochemical manufacturing. Ilya Raskin, Rutgers University The post-industrialized agricultural biotechnology era: what’s rate limiting? John Ryals, Paradigm Genetics, Inc. Transgenic plants for the tropics: some strategies to develop them and reach the farmer. Luis Herrera-Estrella, Centro de Investigacion y Estudios Avanzados, Irapuato, Mexico Panelists: Donald Roberts, Boyce Thompson Institute; Ron Sederoff, North Carolina State University; Roger Beachey; The Scripps Research Institute; Dennis Avery, Hudson Institute; Richard Meagher, University of Georgia; Brian Staskawicz, University of California, Berkeley. Sunday, Dec 6, 1998 Session IV: Biodiversity and multiple land use demands Chair: Dr. Harold Mooney, Stanford University From prehispanic to future conservation alternatives: lessons from Mexico. Arturo Gomez-Pompa, University of California, Riverside Gardenification of tropical conserved wildlands: multitasking, multicropping and multiple users. Daniel Janzen, University of Pennsylvania Plant biodiversity, land use, and the sustainability of essential ecosystem services. David Tilman, University of Minnesota Food supply expansion and the sustainable global management of carbon and nitrogen: interacting challenges. Robert Socolow, Princeton University Panelists: Paul Ehrlich, Stanford University; Wes Jackson, The Land Institute; Thomas Lovejoy, Smithsonian Institution; Walter Reid, World Resources Institute.

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TABLE OF CONTENTS

v

P ROCEEDINGS OF THE

N ATIONAL A CADEMY OF S CIENCES OF THE U NITED S TATES OF A MERICA

Table of Contents

Papers from a National Academy of Sciences Colloquium on Plants and Population: Is There Time?

Plants and population: Is there time? Nina V. Fedoroff and Joel E. Cohen

5903–5907

World food and agriculture: Outlook for the medium and longer term Nikos Alexandratos

5908–5914

The growth of demand will limit output growth for food over the next quarter century D. Gale Johnson

5915–5920

Global and local implications of biotechnology and climate change for future food supplies Robert E. Evenson

5921–5928

World food trends and prospects to 2025 Tim Dyson

5929–5936

Plant genetic resources: What can they contribute toward increased crop productivity? David Hoisington, Mireille Khairallah, Timothy Reeves, Jean-Marcel Ribaut, Bent Skovmand, Suketoshi Taba, and Marilyn Warburton

5937–5943

Ecological approaches and the development of “truly integrated” pest management Matthew B. Thomas

5944–5951

Ecological intensification of cereal production systems: Yield potential, soil quality, and precision agriculture Kenneth G. Cassman

5952–5959

The transition to agricultural sustainability Vernon W. Ruttan

5960–5967

Biotechnology: Enhancing human nutrition in developing and developed worlds Ganesh M. Kishore and Christine Shewmaker

5968–5972

Use of plant roots for phytoremediation and molecular farming Doloressa Gleba, Nikolai V. Borisjuk, Ludmyla G. Borisjuk, Ralf Kneer, Alexander Poulev, Marina Skarzhinskaya, Slavik Dushenkov, Sithes Logendra, Yuri Y. Gleba, and Ilya Raskin

5973–5977

Transgenic plants for tropical regions: Some considerations about their development and their transfer to the small farmer Luis Herrera-Estrella

5978–5981

From pre-Hispanic to future conservation alternatives: Lessons from Mexico Arturo GómezPompa and Andrea Kaus

5982–5986

Gardenification of tropical conserved wildlands: Multitasking, multicropping, and multiusers Daniel Janzen

5987–5994

Global environmental impacts of agricultural expansion: The need for sustainable and efficient practices David Tilman

5995–6000

Nitrogen management and the future of food: Lessons from the management of energy and carbon Robert H. Socolow

6001–6008

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TABLE OF CONTENTS vi

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PLANTS AND POPULATION: IS THERE TIME?

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This paper is the introduction to the following papers, which were presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5–6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Plants and population: Is there time?

NINA V. FEDOROFF * † AND JOEL E. COHEN ‡ and

HISTORICAL BACKGROUND The year 1998 was the 200th anniversary of the publication of Malthus’s famous first essay on population (1). Malthus argued that agriculture could not increase production as fast as the lust between the sexes would inevitably increase population size, and therefore that humans were condemned to poverty, famine, pestilence, and vice. Malthusian worries have been echoed by many since Malthus first wrote. Today discussions about the future growth of food supply and population are increasingly informed by the awareness that human activities impinge on the Earth’s ability to sustain them. There is concern about the ecological and environmental consequences of expanding the food supply further to feed the still rapidly growing numbers of humans. In 1968, a young Stanford biologist named Paul Ehrlich published a short book called The Population Bomb (2). This widely read book warned of the dangers of continuing rapid population growth, especially in the poor countries of the world. In the same year, 1968, J. George Harrar, President of the Rockefeller Foundation, gave a talk entitled “Plant Pathology and World Food Problems” before the First International Congress of Plant Pathology in London (3). Harrar celebrated the cultural and material achievements of humans but emphasized the need for scientists to help solve the persistent problems of “wars, . . . , hunger, poverty, disease, ignorance, social and cultural deprivation, and overpopulation.” Harrar noted that there were then just under 3.5 billion people in the world and anticipated 6 billion by the year 2000. He urged the development of improved forms of contraception. “If there is evidence that birth rates can and will be reduced, vast effort to augment world food supplies will then become increasingly meaningful” (ref. 3, p. 587). Harrar described the past contributions of plant pathology to the increase of crop production and the need to apply recent progress in biology to increase food production. “Genetic manipulation of plant species is as old as plant breeding, but its modern aspects offer exciting new possibilities for disease control as well as for greater productivity. It is becoming increasingly possible to map and identify the genes controlling a variety of functions and to introduce or extract genetic factors for a variety of traits, including disease resistance, increased yields, tolerance to heat, cold, and drought, photoperiod insensitivity, and increased amino acid content of food products. Currently, efforts are also being made to collect, identify, and store genes. Scientists can then draw on these ‘germplasm banks’ as they are needed” (ref. 3, p. 593). After discussing “one highly interesting form of biological engineering,” the then new IR8 rice variety, “which has been remarkably successful in most rice-producing regions,” Harrar noted public concern about problems of food and population. He concluded “with cautious optimism.” His optimism was limited by “the alarming fashion in which scientific and social advances are changing the quality of our environment, [including] the destruction of our soils and water courses, negative interference with the food cycle, and positive pollution of our air envelope . . . Agriculture, too, complicates the ecological pattern . . .” Thus “scientific and social advances” were and are accompanied by negative as well as positive effects. The challenge of finding a desirable balance among the inevitable tradeoffs remains. In retrospect, Harrar’s assessment seems surprisingly prescient and modern. The rice variety IR8 was a leading entry in the Green Revolution. Complex changes in varieties planted, farmer education, farm management, credit institutions, agricultural extension, irrigation, and chemicals applied as biocides and fertilizers combined to increase food production faster than population grew in certain areas. Since 1968, despite rising total numbers of people, increased food production and changes in the distribution of access to food have reduced the absolute number and the fraction of people estimated to be chronically undernourished in every region of the world except sub-Saharan Africa. Yet despite this remarkable progress, an estimated three-quarters of a billion people still suffer from undernutrition.

DEMOGRAPHIC SITUATION AND PROSPECT: THE CHALLENGE The global population growth rate reached an all-time high of 2.1% per year just as Ehrlich and Harrar were writing. The annual rate of increase has since declined by about one-third to roughly 1.4% (4). Global population size is expected to pass 6 billion in 1999. Apart from the catastrophic effects of AIDS across the middle of Africa and the collapse of the economy of the former Soviet Union, life expectancies have increased almost everywhere, indicating overall better human health. These increases in life expectancy are largely attributable to improvements in sanitation, diet, reductions of environmental hazards, behavior, and, to a limited extent, improvements in medical care. The clouds that Harrar foresaw on the environmental horizon have cleared in some places and darkened in others. Although the quality of air and water have improved in some developed countries, they have deteriorated in many less developed countries. Moreover, in some areas, withdrawals of water for agriculture are unsustainable; in many places, water use in agriculture is both technically and economically inefficient. The adverse effects of treating common resources (such as marine fisheries, water supplies, biological diversity, the atmosphere, and some land and forest areas) as unlimited and free have become more evident. Human interventions in global geochemical cycles of water, nitrogen, carbon, methane,

* † ‡

Biotechnology Institute, The Pennsylvania State University, University Park, PA 16802; To whom reprint requests should be addressed. e-mail: [email protected] . Laboratory of Populations, Rockefeller University and Columbia University, New York, NY 10021-6399

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PLANTS AND POPULATION: IS THERE TIME?

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and other compounds and elements have outpaced scientific capacity to anticipate reliably the effects of these interventions. Will the food supply keep up with human population growth over the next half century, and if so, at what costs to other aspects of the quality of life for present and future generations? Answers will depend on economics, environments, and cultures as much as on population sizes. Answers will differ depending on whether the query is local, national, or global. Nevertheless, it is helpful to start with a rough picture of population sizes that can reasonably be anticipated, as well as their distribution. Currently the global population of nearly 6 billion is increasing by about 80 million people per year. Were growth to continue at this annual rate of 1.4%, the population size would double to 12 billion in roughly 50 years. Most demographers view this scenario as unlikely because the rate of increase in population size has been declining for several decades and the absolute number of people added annually to the global population has been dropping since roughly 1990. It now appears unlikely that 6 billion more people will be added to today’s 6 billion. At the opposite extreme, if the annual increase in population were to drop linearly from today’s 80 million to zero over 50 years, then the average annual increase would be 40 million per year for 50 years. Population would increase by 2 billion people to give a population size of 8 billion in the year 2050. This optimistic scenario requires continuing and accelerating declines in fertility in presently poor countries with high fertility rates. Between these extremes, it is plausible to imagine a population size in 2050 of 9 or 10 billion (5, 6). Remembering that the human population numbered only 3 billion as recently as 1960, these numbers can only be viewed with awe. In 1998, roughly 1.2 billion people—one person in five— lived in the developed countries, defined as North America north of the Rio Grande, Europe, Japan, Australia, and New Zealand, and sometimes including some smaller Asian countries. Most of these countries have fertility rates below replacement levels (6) and little if any of the next half century’s population growth is expected to occur in these countries. But unless the pace of economic and educational development accelerates markedly, the fraction of people living in developing countries will increase from 4 in 5 at the end of the 20th century to as many as 9 in 10 by 2050. The population density in the developed countries is currently about 22 people per km2, whereas that in the developing countries is roughly 55 people per km2. The latter number will roughly double to 100 people per km2 if global population grows to 10 billion, largely as a result of increases in the developing countries. This is one person per hectare. Attaining acceptable qualities of life in developing countries at such population densities will be a challenge of unprecedented proportions. About 3 billion people presently live in the rural areas of developing countries. According to some demographic projections, this number is not expected to change much over the next half century, whereas the number of urban people in developing countries is expected to grow enormously, by as many as 3–5 billion (5). If these expectations are realized, then in the developing world roughly the same number of rural people will have to provide a very much larger number of urban people with food and fiber or these products of agriculture will need to be acquired from the developed world by trade or gift. In 1998, the distinguished Australian plant physiologist Lloyd T. Evans reviewed the intertwined history of human population growth and agricultural development (7). He wrote: “. . . not only has agricultural evolution made increase in population possible—indeed it has been blamed for it—but also . . . population growth has driven the development of agriculture. . . . [Nevertheless,] the path to feeding the ten billion in a sustainable way is still by no means clear.”

COLLOQUIUM GOALS AND STRUCTURE The National Academy of Sciences Colloquium titled “Plants and Population: Is there time?” was organized to shed light on how the world will feed its still expanding population in a sustainable way while maintaining enough wildlands to support and preserve essential ecosystems services and biodiversity. The magnitude and activities of the human population make the task more complex than ever—and more critical. The Colloquium brought together economists, demographers and other social scientists, as well as agronomists, biotechnologists, geneticists, and ecologists. Ismail Serageldin, the Vice President for Special Programs of the World Bank, provided a forward-looking overview in his after-dinner address. He emphasized that the currently rich countries have agricultural and institutional needs that differ importantly from those of the currently poor countries. The responses of the rich countries will not automatically satisfy the needs of the poor. He emphasized the need to design an international system of intellectual property that balances the private-property interests of the rich countries with the public-good needs of the poor. The four scientific sessions focused on: demographic and economic projections of food demand and supply; limits on land, water, energy, and biological resources in agriculture; plant biotechnology; and biodiversity and multiple land use demands. Dominated by representatives of a single discipline, each session produced a markedly different vision of our planetary future.

INSIGHTS FROM THE COLLOQUIUM Different disciplines approached the Colloquium’s central question from very different perspectives, made widely different assumptions, and applied different yardsticks to measure success. Participants’ spirits were alternately lifted by projections of sustained expansion of productivity and of as yet barely imaginable improvements in both the health and healthfulness of crop plants, then dashed by predictions of the swiftly approaching limits of plant productivity, constraints on the availability of land, water, and other resources, and threats to the sustainability of natural and anthropogenic ecological processes and systems. The first session, dominated by economists, examined the forces that shape agricultural production today. Cereal production per person world-wide peaked in the mid-1980s, declined over the next decade, then began to grow again in the mid-1990s, according to speaker Nikos Alexandratos. Historical economic analyses showed that the decline, far from being a first harbinger of inadequate world food supply, was largely the result both of deliberate efforts to decrease overproduction in Europe and North America, where prices fell because production capacity exceeded demand, and of the collapse of the Soviet Union. Intentional cutbacks in production, despite persistent undernutrition in some parts of the world, resulted from the difference between effective demand—cash exercised in the market—and the need for calories and nutrients adequate for health, which does not depend on income. Speaker Tim Dyson addressed the profound differences in progress toward food self-sufficiency in different parts of the world. Speaker Gale Johnson pointed out that low grain prices on world markets have been a signal for some governments and international donors to reduce support of agricultural research, thereby hampering the capacity of the agricultural system to respond to future changes. Dyson noted that much agricultural research has bypassed Africa, where needs for additional food are most acute. Speakers Tim Dyson, Robert Evenson, Gale Johnson, and Nikos Alexandratos all agreed that the growth in the world’s effective demand for food with increasing population could be

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met by the world’s agricultural system as a whole, although they differed in the optimism of their projections. Alexandratos reported projections that the average cereals yield of the developing countries would grow at 1.5% per year until 2010, down from 2.2% per year in the past. Based on macroeconomic projections that the currently poor countries will not achieve the levels of income of the currently rich countries within the next few decades, Alexandratos pointed out that a decline in global cereal production per person will not necessarily mean an equivalent decline in the average calories consumed per person. This apparent paradox arises because population will grow predominantly in the less developed countries where people consume three to four times fewer primary plant calories per day (as plant and animal products) than do people in developed countries. These projections assume, therefore, that current differences between countries in primary caloric consumption rates will persist. All of the speakers in this session acknowledged that population increases in some of the least agriculturally productive countries were not likely to be met by local increases in production and would require increased transfer of agricultural products through trade. How the less developed countries would become rich enough to buy the food required to feed their people was not addressed. However, speaker Robert Evenson emphasized that delaying the development and use of biotechnology to increase local grain yields would adversely affect poor countries far more than rich. Participants in the second session, drawn from agronomy, plant breeding, agricultural economics, ecology, and other disciplines, addressed what would be required for world agriculture to continue the yield increases of recent decades. Speaker Vernon Ruttan pointed out that many of the gains in yield that could easily be imagined half a century ago have now been achieved. These gains were attributable to spectacular increases in crop planting density made possible by changes in plant architecture, marked jumps in harvest indices (the weight of usable food product as a fraction of total plant weight), transitions to harvesting multiple crops per year in many areas, introduction of strains with greater responsiveness to fertilizer, improvements in management practices, and expansion of irrigated area. Many of these improvements cannot be repeated. Panelist Thomas Sinclair emphasized that plants’ ability to capture and fix energy is inherently limited by the physics of intercepting photons and capturing carbon dioxide, the biochemistry of photosynthesis, and the physiology of nutrient uptake and utilization. Although perhaps ultimately changeable, it is not clear that these limits can be changed rapidly enough to keep food production ahead of need and demand. The extraordinary agronomic improvements of recent decades have moved present agriculture closer to theoretical limits. Speaker Kenneth Cassman presented evidence that the yield potential of two of the three most important cereal crops, rice and maize, has changed little in response to plant breeding in the past three decades. He argued that the performance of cereals was reaching 80% of theoretical limits in some geographic areas already, and that continuing increases in productivity per hectare would occur only if average yields achieved by farmers rose to comparable levels in the major cereal production systems worldwide. He suggested that although this rise might be attainable, it would require a profoundly deeper understanding of crop physiology and soil science than we now have. Information-intensive management of inputs and natural resources will be required to achieve these yield levels while preserving environmental quality. Speaker David Hoisington suggested that major gains in productivity could still be made by accelerating the transfer of plant genes from diverse sources by using the techniques of molecular biology. Speaker Matthew Thomas argued that productivity could be increased immediately and substantially by pest management that takes better account of all interactions among plants, herbivorous insect pests, and natural enemies of pests. Local ecological interactions need to be understood better in the context of larger ecosystems. The effects of biotechnology and gene manipulations on a single plant or at one site are an inadequate basis for effective area-wide prescriptions. Thomas and panelist William Murdoch noted that more analytical work could be done on past biological control efforts to derive information that could improve future ones. Panelist Vaclav Smil pointed out that a large fraction of food is still lost to spoilage and waste and suggested that significant food gains could still come from improvements in postharvest storage and distribution systems. Panelist Catherine Woteki emphasized the need for more attention to the production of a health-promoting mix of crops and to the safety of crops for consumers. Overall, the second session brought the sobering realization that future productivity gains would be more difficult to achieve than past gains and would require more basic knowledge, better institutional support, and increasingly sophisticated management practices. Optimistic presentations by molecular biologists in the third session sought to dispel an earlier undertone of pessimism about the potential of biotechnology. Speaker Ganesh Kishore articulated a vision of a future for agriculture and human health based on a combination of information technology and biotechnology. He spoke of crops that will produce food better suited to the nutritional needs of both humans and animals, will remedy widespread nutrient deficiencies, will improve human health, and will protect environmental quality. He reported that unanticipated yield increases have already resulted from the new weed management practices used with genetically engineered herbicideresistant soybeans. Speakers Kishore and John Ryals noted that transgenic crops expressing the insecticidal Bacillus thuringiensis endotoxin gene also showed surprising increases in productivity, apparently because reduced insect damage indirectly increases disease resistance. Ryals sketched out the rapid progress in plant genomics that promises to make available an unprecedented variety of individual plant genes useful for improving crop plants. Speaker Ilya Raskin described uses of plants to remediate environmental pollution and produce nonfood products. Plants can extract and concentrate compounds from the soil to clean up land and water contaminated with uranium and other heavy metals. Plants also have the potential to become low-input biological factories through their ability to secrete small molecules and macromolecules into the surrounding medium. Panelist Richard Meagher described using bacterial genes to create transgenic plants that detoxify mercury-contaminated soils. Panelist Brian Staskawicz discussed recent progress in identifying plant disease-resistance genes. He expected that impending understanding of underlying molecular mechanisms would soon make it possible to enhance many different crop plants with durable disease resistance very quickly by genetic engineering techniques. Speaker Luis Herrera-Estrella concluded the session with an assessment of the disparate biotechnological needs of agriculture in differently developed countries. He pointed out that, compared with developed countries, the developing countries have many more small farmers, a different interdependence of culture and agricultural practices, and a variety of problems, many of which are of little interest to the agronomic and biotechnological sectors of developed countries. For example, acid soils comprise 40% of the world’s arable land. A common problem in the acid soils of many tropical countries is high levels of aluminum. Herrera-Estrella described recent success in making local crop plants that tolerate high soil aluminum levels by introducing bacterial genes that enhance the plants’ ability to secrete small organic acid molecules to chelate the

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aluminum. He articulated the need to accelerate the transfer of biotechnology from developed to less developed countries by easing restrictions on intellectual property rights, which increasingly limit the use of each component of a gene construct. He argued that biotechnology could make a culturally acceptable contribution to the welfare of small farmers if the yields of local varieties could be increased through genetic engineering. Export taxes could pay back biotechnology companies holding the patents if productivity increased enough for farmers to export produce. Panelist Donald Roberts pointed out that one-third of the world’s food is not cereals. In West Africa, cassava has replaced maize as the staple subsistence crop. He suggested that noncereal crops deserve more attention from biotechnologists. Herrera-Estrella’s emphasis on improving food production among poor farmers with small areas to cultivate reinforced a point raised in earlier discussion. Several of the economists, including panelist Kenneth Arrow, pointed out that today’s chronic widespread hunger results largely from inadequate cash incomes among the poor, not from inadequate global production of food. Given appropriate governmental policies, increasing the capacity of poor farmers to grow food could raise their incomes at the same time that it would increase the local food supply. Apart from the effects of chronic poverty, acute widespread hunger today often results from the breakdown of public order because of civil wars or other violent political instability. The fourth and final session, dominated by ecologists, focused on the larger environment. The human population and its activities bring different demands on natural resources into conflict. Water management practices are inadequate to cope with sometimes mutually exclusive demands from agriculture, industry, and urban populations. Speaker Robert Socolow identified a need to assess and manage the global nitrogen cycle, just as ongoing efforts are devoted to assessing and managing the global carbon cycle. Nitrogen from agriculture and the burning of fossil fuels contributes to greenhouse gases, stratospheric ozone depletion, and eutrophication and can result in the effective sterilization of coastal waters through oxygen depletion. Based on an analysis of trends in the past 35 years, speaker David Tilman suggested that another doubling of agricultural production will have profound effects on non-agricultural ecosystems because of massive inputs of nitrogen and phosphorus, and because nonagricultural ecosystems will have to be converted to agriculture. Panelist Ronald Sederoff pointed out that current projections fail to take account of the growing demand for wood and wood products, particularly paper. The demand is likely to be met in the future only if trees are domesticated and rapidly growing varieties are developed and farmed. Several participants, including speaker David Tilman and panelist Wes Jackson, stressed the vulnerability of monocultures, which dominate agricultural practices in developed countries. Tilman and Jackson encouraged greater crop diversity to decrease the risk of crop failure. But speaker Daniel Janzen pointed out that monocultures occur throughout nature in a wide variety of circumstances, and Ruttan pointed to examples of monocultural systems, such as east Asian wet rice culture, that have been sustained over several centuries. Other participants noted that in both natural plant communities and agriculture, a mixed culture can produce more biomass per unit area than a monoculture because of partitioning of utilization of resources. Panelist Dennis Avery emphasized that our future ability to maintain current wildland area and meet the food needs of the still growing human population depends on further increases in the productivity of the land already under cultivation. Indeed, the net area under cultivation worldwide has changed very little over the past 30 years. Most of the best land is already in cultivation, and additions are generally offset by losses to urbanization, salinization, and desertification. Thus the goal of increasing food production while preserving current wildland area requires future crops and crop systems to be more productive per unit of land area than are today’s. The alternative of major increases in the area under cultivation would have significant social and economic costs, as well as negative ecological impacts. Speakers Arturo Gomez-Pompa and Daniel Janzen considered how to integrate conservation efforts throughout the world with the support of local, national, and international populations. Janzen warned that tropical wildlands would survive only if tended as multipurpose “gardens.” These gardens should provide protective stewardship for and access to biodiversity as well as essential ecological services and should receive payment for the goods and services they provide. Janzen proposed new mechanisms to generate income from both biodiversity and ecological services and stressed the importance of returning income to the local stewards of the gardens. There were profound and sobering differences of opinion about humanity’s future ability to feed the human population while sustaining ecosystem services and preserving wildlands. The question has changed and grown more complex as the magnitude and impact of human activities have expanded. Panelist Walter Reid pointed out that when the scale of agriculture was small, and undisturbed ecosystems were vast, the underlying ecosystems seemed limitless, and what has recently come to be called their “services” could be freely available to everyone. Humans concentrated on optimizing food supply, often with little concern for the ecological consequences. Now the competing demands of the human population for ecosystem services and the direct and indirect environmental costs of our activities are no longer negligible. Yet efforts to value the planet’s ecosystem services are relatively new, controversial, and have as yet had little real impact.

CONCLUDING PERSPECTIVE The Colloquium must be viewed as a step near the beginning, not the end, of a journey. Both more knowledge and better institutions will be required to continue the journey toward a better fed world. The Colloquium focused on food production and sustainability, leaving equity and other aspects of the quality of life for future discussion. We lack the knowledge to resolve the differences in perspective that startled many participants in the Colloquium. Many questions raised during discussion went begging for answers. How reliable are global statistics on the extent of hunger, the extent of desertification, the amount of land used for agriculture? How and how much does soil erosion impair agriculture in various parts of the world? How much carbon and nitrogen must farmers return to the land from crops to maintain optimum soil fertility? How rapidly will resistance to pesticidal proteins, such as the Bacillus thuringiensis endotoxin, emerge in insect pests? How can intellectual property rights be managed to optimize the balance between the interests of biotechnology firms in developed countries and poor farmers in developing countries? How extensive are postharvest losses of food? How can the existing information about improved farming practices and materials be diffused more effectively to farmers in countries with very different levels of education and technological sophistication? How important to food production are regional variations in topography, climate, soil, biotic environments, institutions, and individual behaviors? Which are the best targets for intervention? If there are substantial uncertainties about future climate change and about the effects of each possible change on agricultural production, what strategies of response make the most sense for national governments and international organizations?

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We also lack the human institutions required to define, develop, integrate, and apply the requisite knowledge. Ruttan wrote: “If the world fails to meet the challenge of a transition to sustainable growth in agricultural production, the failure will be at least as much in the area of institutional innovation as in the area of resource and environmental constraints. . . . At our present stage of knowledge, institutional design is analogous to driving down a four-lane highway looking out of the rear-view mirror. We are better at making course corrections when we start to run off the highway than using foresight to navigate the transition to sustainability.” Panelist Dennis Ahlburg further pointed out that we do not know how to design “better policies” like market reforms, as experience in Eastern Europe attests. Where are useful models for developing the institutions and knowledge needed to manage agricultural and wildlands in a way that sustains global ecosystem services and promotes human well-being? Although the Earth’s biogeochemical cycles ensure that local practices have distant and even global impacts, our thinking is far from integrative and global. Scientific models are just beginning to grapple with the realization that complex systems, whether geological, biological, or human, often exhibit nonlinear responses. These include abrupt shifts in oceanic circulation and climate, mutations that increase the virulence of pathogens, extinctions of species, and rapid changes in human fertility, mortality and migration. In addition, dilemmas of population, equity, food, and environmental quality are local in many important respects, as panelist Billie Lee Turner emphasized. These realizations must inform our information-gathering, our institution-building, and our thinking about the kinds of changes that would lead to sustainable practices in agriculture and all other spheres of human activity. Our ability to gather local data on a global scale and to work locally while integrating our activities across vast geographic distances has never been better. It will continue to improve in the future as satellite imaging techniques develop and computer networks expand. Molecular biology and biotechnology open new vistas for understanding and altering the properties of all organisms on which humans depend, including plants. The potential pace of change could not even have been imagined 30 years ago. Whether and how this potential is realized—and whether it is accepted by people—cannot yet be foreseen. Finding solutions will require collaborative efforts of a broad array of disciplines and constituencies. Success will depend profoundly on what we do now and in the immediate future. What is very clear is that there is no time to lose. A previous draft of this summary was sent for review to all speakers and panelists in the Colloquium. We thank the following for helpful comments: Dennis Ahlburg, Nikos Alexandratos, Kenneth Cassman, Tim Dyson, Paul R. Ehrlich, Daniel Janzen, William Murdoch, Walter Reid, Don Roberts, Vernon Ruttan, Robert Socolow, Matthew Thomas, David Tilman, and Catherine Woteki. We thank the National Academy of Sciences for sponsoring this Colloquium. J.E.C. acknowledges support of National Science Foundation Grant DEB9207293. 1. Malthus, T. R. (1798/1970) An Essay on the Principle of Population, ed. Flew, A. (Penguin , London). 2. Ehrlich, P. R. (1968) The Population Bomb (Ballantine Books , New York ). 3. Harrar, J. G. (1970) Persp. Biol. Med. 13, 583–596 . 4. Population Reference Bureau (1998) 1998 World Population Data Sheet (Population Reference Bureau , Washington, DC). 5. United Nations, Population Division (1997) Urban and Rural Areas 1996 (United Nations , New York), Publication ST/ESA/SER. A/166 . 6. United Nations, Population Division (1998) World Population Estimates and Projections, 1998 Briefing Packet (United Nations , New York). 7. Evans, L. T. (1998) Feeding the Ten Billion: Plants and Population Growth (Cambridge Univ. Press , Cambridge, U.K.).

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

World food and agriculture: Outlook for the medium and longer term

NIKOS ALEXANDRATOS Global Perspective Studies Unit, Food and Agriculture Organization, Rome 00100, Italy ABSTRACT The world has been making progress in improving food security, as measured by the per person availability of food for direct human consumption. However, progress has been very uneven, and many developing countries have failed to participate in such progress. In some countries, the food security situation is today worse than 20 years ago. The persistence of food insecurity does not reflect so much a lack of capacity of the world as a whole to increase food production to whatever level would be required for everyone to have consumption levels assuring satisfactory nutrition. The world already produces sufficient food. The undernourished and the food-insecure persons are in these conditions because they are poor in terms of income with which to purchase food or in terms of access to agricultural resources, education, technology, infrastructure, credit, etc., to produce their own food. Economic development failures account for the persistence of poverty and food insecurity. In the majority of countries with severe food-security problems, the greatest part of the poor and food-insecure population depend greatly on local agriculture for a living. In such cases, development failures are often tantamount to failures of agricultural development. Development of agriculture is seen as the first crucial step toward broader development, reduction of poverty and food insecurity, and eventually freedom from excessive economic dependence on poor agricultural resources. Projections indicate that progress would continue, but at a pace and pattern that would be insufficient for the incidence of undernutrition to be reduced significantly in the medium-term future. As in the past, world agricultural production is likely to keep up with, and perhaps tend to exceed, the growth of the effective demand for food. The problem will continue to be one of persistence of poverty, leading to growth of the effective demand for food on the part of the poor that would fall short of that required for them to attain levels of consumption compatible with freedom from undernutrition.

KEY HISTORICAL DEVELOPMENTS Improvements in Food Supplies. In the last three decades, the world as a whole has made significant progress in the food and nutrition area. Progress is measured in terms of the per person availability of food products for direct human consumption as a national average in each country, expressed in kcal/day. This is an admittedly imperfect yardstick. However, it comes much closer to what we need to measure and monitor—the degree of satisfaction of human food needs— than the commonly used measure of gross production of food commodities per person. Gross production ignores postharvest losses and all uses of food commodities other than for direct human consumption, e.g., for seed, animal feed, and ethanol production (from maize in the USA and sugar cane in Brazil). * By accounting fully for food imports and exports, per person availability makes possible the monitoring of changes in the apparent food consumption of individual countries, which the production statistics alone cannot do. As a world average, the per person food availability for direct human consumption grew 19% to 2,720 kcal/day (1 kcal = 4.18 kJ) in the 35 years to the 3-year average 1994–1996, whereas that of the developing countries grew 32% to 2,580 kcal/day. † Meanwhile, world population grew from 3.0 billion in 1960 to 5.7 billion in 1995. Naturally, world averages have limited value for tracking changes in the welfare of persons (see below). Use of the national averages of individual countries makes possible the analysis of intercountry distribution of gains. As such, the national averages provide a better, although far from satisfactory, basis for tracking such changes. They show that the part of world population living in countries where per person food supplies are still very low (under 2,200 kcal/day) decreased considerably to only 10% in the mid-1990s, down from 56% 30 years earlier. At the other extreme, 60% of the world’s population now lives in countries with per person food supplies over 2,700 kcal/day, up from 30% 30 years ago. China, with its huge population and rapid economic and agricultural growth after the late 1970s, accounts for a significant part of this massive upgrading in the food availability of the developing world. Excluding China, the gains of the developing countries have been much less impressive, 22% rather than 32%. The detailed country-level data indicate that progress has been very uneven and has bypassed a large number of countries and population groups. Many countries in subSaharan Africa and South Asia and assorted countries in other regions either made little progress or suffered outright declines from levels that were grossly inadequate for good nutrition to start with. Thus, sub-Saharan Africa still has food availability of only 2,150 kcal/day, compared with 2,050 kcal 30 years earlier. The comparable figures for South Asia are 2,350 kcal and 2,000 kcal, respectively. The per person food availabilities of the other developing regions (Latin America/Caribbean, East and Southeast Asia, and Near East and North Africa) are in the range 2,700–3,000 kcal, whereas those of Western Europe and

PNAS is available online at www.pnas.org. It is, however, inclusive of post-retail waste and nonfood uses at the household level, e.g., food fed to pets—hence the very high levels of food availability generally found in the statistics of many high-income countries, often over 3,500 kcal·person−1·day−1. † The term developing countries comprises all of the countries of the world except those of Europe (both east and west) and North America, all the countries of the former U.S.S.R., Japan, Australia, New Zealand, the Republic of South Africa, and Israel. This classification reflects, above all, traditional practice and is useful for historical comparisons. However, it leaves much to be desired when it comes to grouping countries by levels of development currently prevailing, a problem that has been intensified in recent years with the new low-income countries created in the wake of the collapse of many economies formerly centrally planned. *

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North America are 3,370 kcal and 3,570 kcal, respectively (see footnote †). The extremely low levels of food availability still prevalent in several developing countries imply that undernutrition is widespread. It is estimated that there are currently over 800 million persons undernourished in the developing countries, with high concentrations in South Asia and sub-Saharan Africa (1). Progress in reducing these numbers has been painfully slow, with reductions in East Asia being compensated to a large extent by increases in sub-Saharan Africa. The Role of Food Trade. The bulk of the increases in the consumption of the developing countries was met by increases in their own production. In the case of cereals, their production grew at 3.0% per annum (p.a.) in the 3 decades to the mid-1990s and provided 87% of the increase in their consumption. However, in a considerable number of countries, gains in food availability depended to a significant degree on rising food imports, particularly during the 1970s. In that decade, the net imports of cereals of the developing countries as a whole tripled, following the growth of incomes and foreign exchange earnings of the oil exporters, as well as the conditions of easy foreign borrowing and debt accumulation of other countries. For example, in North Africa, the per person consumption of cereals (all uses) increased from 232 kg in the mid-1960s to 322 kg in the mid-1980s, and per person net imports skyrocketed from 44 kg to 167 kg in the same period. North Africa’s cereals self-sufficiency (production as percentage of consumption) fell from 76% to 51% in the 2 decades to the mid-1980s and has remained in the range 50–55% in subsequent years. Many other countries experienced similar precipitous declines in their self-sufficiency associated with improvements in consumption over the same period, e.g., Saudi Arabia, Republic of Korea, Taiwan Province of China, Congo, and Gabon. Not all developing countries went through this experience of growing dependence on imports, certainly not the largest ones. The two most populous countries of the world, China and India, illustrate this point. China, widely discussed in recent years as a potential source of huge increases in import demand in the future (2, 3), had net imports of cereals exceeding 5% of its aggregate consumption only in exceptional years during the period of quantum gains in its domestic demand. More often it was close to 100% self-sufficiency, and China was an occasional net exporter. India, which depended on cereal imports for a crucial 14% of its consumption 30 years ago and was widely believed to be on a path of growing dependence on such imports, became virtually 100% self-sufficient and indeed an occasional net exporter. India’s apparent consumption of cereals grew at about the same rate as that of China (2.8–2.9% p.a. in the 20 years to 1996), but its gains in per person consumption have been much more modest than those of China, and undernutrition remains widespread. India had started with much lower levels of per person consumption and also had a higher population growth rate than China (2.1% p.a. compared with 1.4% p.a.). Obviously, India’s path of declining dependence on food imports reflected not only the production gains from the green revolution but also the little headway made in reducing poverty and the consequent inadequate growth in the effective demand. Had India achieved gains in per person consumption comparable to those of China, it is an open question whether it would have achieved nearly 100% self-sufficiency. More generally, avoidance of drastic declines in self-sufficiency by the many countries that still have very low levels of consumption often reflects not so much success in their agriculture but rather failure to make sufficient progress toward raising consumption levels to nutritionally satisfactory levels. In conclusion, food imports played an important role in making possible the quantum jumps in consumption of numerous developing countries that could pay for such imports, although the behavior of the very large countries contributed to avoiding large declines in the cereals self-sufficiency of the developing world as a whole. The latter declined from 95% in the mid-1960s to 93% in the mid-1980s and to 90% by the mid-1990s. By about the early 1980s, the era of rapid import growth of the developing countries had come to an end and their net imports moved in the range 70–110 million tons in the subsequent years to the present. These developments notwithstanding, the possibility that there might be further spurts in their import demand is an issue that remained very much alive. It reflects perceptions that there is now much less scope than in the past for further production gains from the green revolution, while sustained economic growth may lift significant numbers of people out of poverty and boost demand at rates high enough to cause a significant part of it to appear as solvable demand for imports (4). From here, it is a short step to worry about the capability of the rest of the world to increase production and generate the necessary export surplus. What does the historical evidence show? By and large, the traditional cereal exporters (North America, Argentina, Australia, and in more recent years, also Western Europe) coped quite well with spurts in import demand. Between themselves, they export currently (average 1994/96) some 160 million tons of cereals net annually. ‡ This is just over 3 times their net exports of 30 years earlier. About one half of the total increment in these net exports was contributed by Western Europe. It is a very significant development for the world food system that this region turned from a net importer of 27 million tons in the mid-1960s to a net exporter by the early 1980s and was exporting 21 million tons net in the mid-1990s. In practice, the other, more traditional, exporters have had (or, perhaps one should say, were constrained by Western Europe’s policies) to increase their net export surplus rather modestly, from 77 million tons in the mid-1960s to about 138 million tons 30 years later. Had Western Europe remained a net importer of 27 million tons, the more traditional exporters would have had to increase their net export surplus to 185 million tons. We do not have a counterfactual scenario to answer the question of how the different variables of the world food system (in particular the per person food availability of the poor countries and those that became heavy importers) would have actually fared if Western Europe had not followed a policy of heavy support and protection of its agriculture. Such policy led to the region’s import substitution and then subsidized exports, all accompanied by polemics and friction in the trade policy area. The resulting lower and more volatile world market prices (compared with what they would have been otherwise) are thought to have adversely affected the food security of the developing countries because of the negative effects on the incentives to their producers. However, the positive effects on the consumption of the poor of the lower import prices and increased availability of food aid must also be taken into account when evaluating the impacts of such policies on food security. In the end, such policies of Western Europe resulted in the emergence of an additional major source of cereal export surpluses to the world markets and diversified the sources from which the importing countries could provision themselves. This is a structural change that is probably here to stay even under the more liberal trade policy reforms of recent years and the further ones to come (5). Slowdown in World Agricultural Growth. In the 1990s, there has been a slowdown in the growth of world agricultural production. World cereals output stagnated and fluctuated widely in the first half of the decade. In per person terms, it fell from the peak of 342 kg achieved in the mid-1980s to a low of 311 kg in the 3-year average 1993–1995, before recovering to

‡ One hundred eighteen to the developing countries other than Argentina, 33 to Japan and Israel, and 6 to the area former U.S.S.R./ Eastern Europe.

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323 kg in the latest 3-year average 1996–1998. In parallel, production of capture fisheries seems to have hit a ceiling of just over 90 million tons, and much of the increase in fish production is coming from aquaculture, a development likely to continue in the future. In the face of these developments, it would appear that the world food situation has been worsening. However, the evidence we presented earlier points in the opposite direction. As noted, world average indicators have limited value for welfare analysis, and the variables must be observed at a more disaggregated level for a correct interpretation. Progress in food security need not manifest itself in rising world averages (i.e., with aggregate production or consumption rising faster than world population), but it is possible for progress to occur when the world average stagnates or even falls. § Thus, in the 10 years to the mid-1990s that witnessed the declines in the world averages, there has been no decline, but rather an increase, in the per person production and consumption of cereals in the developing countries, whereas that of all other food products (roots and tubers, pulses, bananas and plantains, livestock, sugar, oilseeds, fruit and vegetables, etc.) grew even faster than in the preceding 10 years. The problem for the developing countries remains one of too low production and consumption per person. The declines in world cereals output per person have been interpreted by some as beginning an era when the natural resource and technology constraints have become all of a sudden so much more binding (6). In reality, this slowdown has been due, in the first place and up to quite recently, to policy reforms and supply controls coinciding with weather shocks in the main industrial exporting countries. ¶ The longer term deceleration in the growth rate of cereals production in these countries has reflected, above all, the inadequate growth of demand (both domestic and external) for their produce and the associated decline in real prices. For example, the real price of wheat in constant 1990 U.S. dollars per metric ton was in the range of U.S. $200–240 (annual averages) in the first half of the 1980s and in the range of U.S. $125–150 in the following 10 years to 1995. For maize, the ranges were U.S. $150–200 and U.S. $85–105, respectively (ref. 7 and previous issues). In more recent years, the decline reflected also the collapse of production (as well as of consumption and net imports) in the countries of Eastern Europe and the former U.S.S.R. following the drastic systemic reforms in their economies. Although recovery may be long in coming, the collapse of agriculture in this group of countries will likely prove to be a transient phenomenon. What may prove to be a more enduring structural change in the world food system is the impact of policy reforms, in part linked to the new policy environment for international trade. These reforms may lead to the cessation of generation of quasi-permanent structural surpluses and the holding of large stocks in the major exporting countries by the public sector, which in the past were readily available for interventions in case of abrupt shortfalls in supplies.

WORLD PRODUCTION AND FOOD INSECURITY: AN UNCERTAIN LINK. The preceding discussion indicates that, by and large, the production system of the world as a whole has been generating food supplies at a rate which was more than sufficient to meet the growth of effective demand. The evidence is the secular declining trend of the real price of food in world markets (8). It is equally true that food insecurity and undernutrition have persisted at high levels. The combination of these two facts certainly suggests that undernutrition is not because of a lack of global capability to produce the additional food required to eliminate undernutrition, which is a very small amount (2–3%) compared with current or future world food output (9). It is now widely accepted, if there ever was any doubt, that food insecurity and undernutrition are above all caused by the persistence of abject poverty, development failures (often linked to war and unsettled political conditions), and lack of appropriate social policies. This, however, does not absolve us from the need to address the question of the links between food production and the food welfare status of the population, particularly of those countries and population groups with very inadequate consumption levels. Obviously, a prima facie case can be made that such links exist when production failures, particularly where they are endemic, are somehow a causal factor in overall development failures and the perpetuation of poverty. In such cases, it is quite legitimate to hold that persistence of undernutrition is due, at least in part, to inadequate growth of production. Such a statement may not apply to the world as whole but it would be certainly valid in the socioeconomic and natural resource environments in which production failures (or more generally failure to develop agriculture), poverty and undernutrition coexist. Such a link is indeed present in the many low-income countries with high dependence on agriculture (50–80% of the population depending on agriculture as the main source of living). In such situations, failures in agricultural development often lie at the heart of failures in overall development and the persistence of poverty (10). It follows that one of the main thrusts of national and international policies to solve the problem must be the promotion of local food production and broader agricultural and rural development in these countries, so as to simultaneously increase food supplies and stimulate overall development. In conclusion, the widely held view that the persistence of food insecurity and undernutrition is not a problem of production (or production potential) but rather one of distribution (or access, or entitlements) can be both true and false at the same time. It is largely true if it refers to the world as a whole, but this is not a very helpful conclusion. It can be grossly misleading if it induces us to ignore the stark reality that it is often failures to develop agriculture and increase food production locally that lie at the heart of the local food insecurity problem. This is certainly not equivalent to saying that countries in that condition (undeveloped agriculture, often poor natural resource endowments, and large parts of their population dependent on them for a living) have the potential to develop toward middle-income status with an internationally competitive agricultural sector. It rather underscores the need for the path to less poverty, better food security, and eventually freedom from heavy economic dependence on poor agricultural resources to pass precisely through an initial phase of improved agricultural productivity (11). What are the prospects that progress may be made in the foreseeable future (15–30 years)?

§ Simpson’s paradox, meaning that the world can get poorer on average even though everyone is getting richer, simply because the share of the poor in the total grows over time. This can be illustrated as follows (example based on approximate relative magnitudes for the developing and the developed countries): in a population of four persons, one is rich, consuming 625 kg of grain, and three are poor, each consuming 225 kg. Total consumption is 1,300 kg, and the overall average is 325 kg. Thirty years later, the poor have increased to five persons (high population growth rate of the poor) but they have also increased consumption to 265 kg each. There is still only one rich person (zero population growth rate of the rich), who continues to consume 625 kg. Aggregate consumption is 1,950 kg, and the average of all six persons works out to 325 kg, the same of 30 years earlier. Therefore, real progress has been made even though the average did not increase. Obviously, progress could have been made even if the world average had actually declined. Thus, if the consumption of the poor had increased to only 250 kg (rather than to 265), world aggregate consumption would have risen to 1,875 kg but the world average would have fallen to 312.5 kg. ¶ Thus, the European Union (E.U.) production of cereals fell from 191 million tons in the 3-year average of 1989–1991 to 178 million tons in 1993–1995, before growing again to 207–208 million tons in 1996 and 1997 following the high world market prices and the relaxation of supply controls. Production grew further in 1998 to an estimated 212 million tons.

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FUTURE PROSPECTS Demographics, Incomes, and Poverty. One of the key variables determining future outcomes, the growth rate of world population, has been on the decline since the second half of the 1960s. The U.N. demographic assessment of 1996 (12) has a medium variant projection indicating further deceleration, from 1.4% p.a. currently (1995–2000) to 1% p.a. in 2020 and to 0.4% p.a. by the middle of the next century. || However, the absolute increments in world population are currently very large, about 80 million persons p.a., over 90% of whom are added in the developing countries. Such high annual increments (in the range of 70–77 million in the new projections of 1998) may persist for another 15–20 years, but with declines in prospect for the longer term future, falling to some 40 million p.a. (30 million in the new projections) by 2050. Demographic growth in sub-Saharan Africa will increasingly dominate the total additions to world population: it will account for one half of the world increment by 2050, compared with only one fifth currently. On the economic side, the most recent (December 1998) assessment of world economic growth prospects (13) implies that the rate of poverty reduction in the developing countries will be much slower compared with the past, when it was essentially fuelled by the rapid economic growth of East Asia. The growth of this region has been interrupted, and the average of the next 10 years (1998–2007) may be only 2.9% p.a. compared with 7.2% p.a. in the preceding 10 years (1988– 1997) (in East Asia not including China; the fall is much less pronounced if China is included in the region, from 7.4% to 4.8%). On the other hand, South Asia may nearly maintain its past growth rate at the respectable level of 5.4%, a prospect that goes some way toward compensating the loss of poverty reduction momentum emanating from East Asia. At the other extreme, in sub-Saharan Africa, the growth rate of per person income is expected not to exceed 1.0% p.a. This outcome does not augur well for the reduction of poverty and hence undernutrition in the region, even if it reverses the trend of the negative growth rates of the past. Food and Agriculture. These overall economic and demographic prospects form the background against which we must assess the prospects for future progress in food and agriculture. One can say right from the outset that the average world indicators of food availability will register only modest gains. This is because the overall demographic and economic outlook implies that the share of the poor, or rather those with lower-than-average food consumption levels, in the world population is set to continue rising. The food insecurity and undernutrition problems will persist, at somewhat attenuated levels, in the medium term future and perhaps well beyond, in many countries starting with very unfavorable initial conditions (mainly in sub-Saharan Africa and, to a smaller extent, in South Asia and selected countries in other regions). One does not need sophisticated analytics to prove this point: any country starting with per person food supplies of 2,000 kcal/ day (and some countries start with less) and a population growth rate of 2.5–3.0% p.a. would need a growth rate of aggregate food demand of about 5% p.a. for 15 years if, by 2010, it were to have 2,700 kcal/day, a level usually associated with significantly reduced undernutrition (provided inequality of distribution is not too high). Obviously, this kind of growth rates of aggregate demand for food can only occur in countries with “Asiantiger” rates of economic growth sustained over decades. Few of today’s poorest countries with very low food consumption levels face such prospects. As noted, the recent crisis that hit several economies of East and Southeast Asia will also take its toll. The rapid pace of progress of the recent past, particularly in diet diversification toward livestock products, is being interrupted, and some countries (e.g., Indonesia) are suffering outright reversals. These prospects, particularly the demographic ones, are somewhat different from those used some 5 years ago to produce the Food and Agriculture Organization’s assessment of world food and agriculture prospects to 2010, with particular reference to the developing countries, in the study “World Agriculture: Toward 2010” and subsequent modifications used in the technical documentation of the World Food Summit of 1996 (1, 14). However, the essence of our findings as concerns key variables of food security at the level of large country groups and the world as a whole remains largely valid. ** The main findings, including selected preliminary findings from ongoing work to update the study and extend the time horizon to 2015 and 2030, are summarized below. • The per person food availability of the developing countries as a whole will continue to increase from the current (1994–1996) 2,580 kcal/ day to about 2,750 kcal/day by 2010. However, there will be only very modest gains in the currently very low average food availability of sub-Saharan Africa, whereas South Asia may still be in a middling position by 2010. The other developing regions, already starting from better levels now, are expected to be near, or above, 3,000 kcal/day. • The per person consumption of cereals (all uses) of the developing countries may rise from the 245 kg of 1994–1996 to some 260 kg in 2010. The preliminary projections to 2030 suggest a further rise to about 280 kg, whereas the world average will likely reverse its trend toward decline and rise again—from the about 320 kg in the mid-1990s to about 340 kg in 2030. Important in this reversal will be, in addition to the rise of the developing country average, the change of two trends that in the past contributed to its decline: (i) the bottoming out of the declines and the eventual upturn of per person consumption in the formerly centrally planned economies; and (ii) a similar process (already under way) in Western Europe following the policy reforms that lowered domestic cereal prices and reestablished the competitiveness of cereals vis-a-vis cereal substitutes in the feeding of animals. • The incidence of undernutrition in the developing countries may decline in relative terms (from 21% to 12% of the population) but, given population growth, there will be only modest declines in the numbers undernourished. The current level of over 800 million persons is expected to decline to about 680 million by 2010 (1). A high incidence of undernutrition will persist in sub-Saharan Africa, and a

|| The 1996 medium variant projection was for world population to reach 9.4 billion by 2050, up from 5.7 billion in 1995. The just released new U.N. assessment of 1998 shows even more steep deceleration, leading to a world population of 8.9 billion in 2050, about 0.5 billion below that projected in 1996. However, over one half of this reduction (270 million) is in the projected population of sub-Saharan Africa, in part because of the revised estimates of the impact of the AIDS epidemic. As such, this further reduction in projected population is partly associated with negative rather than positive developments in human welfare. **Subject to the great uncertainties concerning the prospects of sub-Saharan Africa, following the drastic revisions of the demographic data. For some countries, not only the projections but also the historical data were revised drastically. For example, in the base year data of the Food and Agriculture Organization Study (14), the 1990 population of Nigeria was given in the 1990 U.N. population assessment as 108.5 million. Four years later (in the 1994 assessment), the population for the same year was given as 96.2 million. The most recent (1998) assessment reduced the 1990 population further to 87 million. One can easily imagine what these revisions imply for the estimates of the key variable of per person food availability and the incidence of undernutrition, a variable which, at low levels of foods availability, is very sensitive to variations of even 5%. The implication is that we shall have to reevaluate where we stand now and where we stood in the past, before we can start talking about the future.

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somewhat reduced one in South Asia. These two regions could account for 68% of the developing country total, up from 56% currently. • Local production increases will be by far the main source of the growth in the food supplies of the developing countries. Their cereals production was projected to grow at 2.1% p.a. from the 3-year average 1988–1990 (the base year of the study) of 845 million tons to 1.32 billion tons in 2010 (wheat, rice in milled form, coarse grains). Nine years into the 21-year projection period, the production of the developing countries had risen to 1,015 million tons (3-year average for 1996–1998) and the growth rate from 1989 to 1998 was as projected, 2.1% p.a. • As in the past, and moreso in the future, the mainstay of production increases will be the intensification of agriculture in the form of higher yields and more multiple cropping, particularly in the countries with appropriate agroecological environments and little or no potential to bring new land in cultivation. As far as possible, we projected yields of the developing countries (other than China) for several agroecological environments. †† The end result of the detailed projections (for individual countries and crops) indicates that the growth of the average yields of the developing countries (other than China) will be slower than in the past, 1.5% p.a. (from 1.9 tons/ha in 1988– 1990 to 2.6 tons/ha in 2010; ref.13, p. 169), compared with 2.2% p.a. in the preceding 20 years (average yield of wheat, rice paddy, and coarse grains). Nine years into the projection period (1989– 1998), the average cereal yield grew as predicted at 1.5% p.a., although rice yield grew by less than predicted, that of maize by more than predicted, and that of wheat as predicted. Continued growth of average yields, even at the lower rates projected here compared with the past, will not come about without effort. Growth in average yields will depend crucially on policies that attach high priority to efforts at agricultural research and technology development and diffusion, as well as on a more active role of the state in the areas of infrastructure, education, and the creation of conditions for markets to work. • Land expansion will continue to be a significant factor in the growth of agriculture in those developing regions where the potential for expansion exists (many countries in sub-Saharan Africa and South America) and the prevailing farming systems and more general demographic and socioeconomic conditions favor land expansion. It is estimated that the developing countries outside China have some 2.5 billion ha of land of varying qualities, which has potential for growing rainfed crops at yields above an “acceptable” minimum level. Of this land, some 720 million ha (plus another 36 million ha of desert land reclaimed through irrigation) are already in cultivation in the developing countries outside China (arable land and land in permanent crops). Most of the remaining 1.8 billion ha is in Latin America and sub-Saharan Africa. At the other extreme, there is virtually no spare land available for agricultural expansion in South Asia and the Near East/North Africa region. Even within the relatively land-abundant regions, there is great diversity among countries and subregions as concerns land availability per person, both quantity and quality. For example, in sub-Saharan Africa, land is scarce in East Africa, and land is relatively abundant in Central Africa. Land expansion may add some 90 million ha to the above estimates of cultivated land of the developing countries (other than China). Such expansion will account for about 20% of the increase in their aggregate crop production. • These projections of areas and yields were arrived at through an examination of the agricultural growth needs and the potentials for land expansion and for technology development and adoption in each country. It would appear that the widely held view that land in agricultural use is not (or will not be) growing any more is probably unduly influenced by the experiences of the industrial countries, and indeed by that of their cereals sector in which area has been on the decline. As noted, this is not the case in those developing countries that combine the above-mentioned characteristics (availability of land, need to expand output and farming systems and, more general socioeconomic conditions favoring land expansion rather than intensification). Otherwise, why should we worry about tropical deforestation caused by, among other things, expansion of agriculture? What does the empirical evidence show? Unfortunately, the quality of the general land use data leaves much to be desired. The data of harvested, or sown, area for the major crops are comparatively more reliable. They show that expansion of harvested area continues to be an important source of agricultural growth in sub-Saharan Africa and South America. In these two regions, the harvested area under the major crops (cereals, oilseeds, pulses) grew 17% in the last 10 years (from average 1986–1988 to average 1996–1998). The comparable increase for the rest of the developing regions was 6%. Moreover, in sub-Saharan Africa and South America, the expansion of area under these crops is likely to have involved bringing new land in cultivation rather than increasing multiple cropping. The latter is not favored by the predominantly rain-fed character of their agriculture. The opposite is likely to have been the case in the other developing regions, where irrigation is very important. • This projected increase of land in agricultural use (some 90 million ha, or 12%, in the developing countries as a whole, excluding China) is a small proportion of the total unused land with rain-fed crop production potential (some 1.8 billion ha). Naturally, such unused land should by no means be considered as a “reserve” for agricultural expansion. As far as we can tell (ref. 13, pp. 155–158), some 50% of it is under tropical forest, and large tracts are environmentally fragile or suffer from other constraints, including lack of infrastructure, incidence of disease, etc. • Concerning the environmental and sustainability dimensions of the expansion and further intensification of agriculture, we note that (i) the foreseen land expansion need not be associated with the rapid rates of tropical deforestation observed in the past, although there is no guarantee that this will be so; (ii) there will be further increases in the use of agrochemicals (fertilizer, pesticides) in the developing countries, although at declining rates compared with the past; (iii) increased use of fertilizer is often indispensable for sustainability (to prevent soil mining); and (iv) the need to accept tradeoffs between production increases and the environment will continue to exist in the foreseeable future and the policy problem is how to achieve such increases while minimizing adverse impacts on natural resources and the wider environment. • The net food imports of the developing countries from the rest of the world should continue to grow, although not at very high rates, i.e., we do not expect major structural surges in the demand for imports like those that occurred in the 1970s (see above). In an earlier version of the study completed in the mid-1980s with time horizon 2000 (15), we had projected net imports of cereals of the developing countries to grow to 112 million tons by the year 2000. The evolution to date indicates that the year 2000 outcome will likely be fairly close to this projection, because net imports have been

†† Problems with the land and yield data of China (3) made it necessary to project the country’s production directly, not in terms of land-yield combinations as it was done for the other developing countries. The resulting projection of China’s production of cereals implies a growth rate of 2.0% p.a. from 1988–1990 to 2010 (ref. 13, p.141). The actual outcome to 1998 has been 2.2% p.a.

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in the range 100–110 million tons in recent years, whereas the current crisis affecting key developing countries does not augur well for an upturn in their import demand. It is expected that there will be some upswing in imports in the next decade, reaching 160 million tons by 2010. The rest of the world should face no major constraints in generating this additional export surplus of cereals, given that (i) the domestic demand of the main exporting countries grows very slowly and below the potential of their agriculture to increase output, and (ii) part of the additional import requirements of the developing countries is being offset by declining import demand of the region of Eastern Europe and former U.S.S.R. This latter region was a heavy net importer in the pre-reform period (some 35 million tons in 1989–1991), but may be a modest net exporter by 2010. The region’s net imports had already been drastically reduced by the mid-1990s, whereas for the trade year July 1997–June 1998, the region is estimated to have been a net exporter of some 3.5 million tons. For the longer term, it is possible to visualize this region emerging as a major additional source of cereal export surpluses in the world (16), just as Western Europe did in the 1980s, although for very different reasons. In the case of the former centrally planned economies, an export surplus will likely be generated from the eventual recovery of agriculture from the status of near-collapse that accompanied radical systemic reforms, rather than from high agricultural support and protection of the type applied in Western Europe. For the longer term beyond 2010, the preliminary findings of the above-mentioned work to update the study and extend its time horizon to 2015 and 2030 indicate that the net cereals exports of the major exporters (North America, Western Europe, Australia, Argentina) would need to approximately double by 2030, from the mid-1990s level of 160 million tons. The required growth rate of their production for generating this export surplus and also meeting the growth of their own demand (including that part of their domestic demand for feed cereals going to produce more meat for export) would be around 1.1% p.a. in the 35 years from 1994–1996 to 2030. This growth rate is well below that achieved in the preceding 35 years (2.0% p.a. in 1961–1996). However, the growth rate of their combined production has been on the decline over time, from 2.8% p.a. in 1961–1986 to 1.2% p.a. in 1986–1996. As noted, this slowdown was mainly the result of lack of demand, falling real prices, and policies put in place to control the growth of production and avoid the accumulation of excessive surpluses. The prospect that the production growth rate in the exporting countries needs to be lower than in the past does not in itself guarantee that it is a feasible proposition. In particular, environmental concerns related to intensive agriculture in the high-income countries (nitrate pollution, soil erosion, perceived risks from genetically modified organisms, etc.) may contribute to slow the rate at which progress may be made in achieving the required yield increases. However, the environmental implications of increased production for export may appear in an entirely different light if examined in a global context, rather than solely in the context of the resource and environmental context of the exporting countries themselves. The global context is provided by the realization that major jumps in the absolute volume of world production are in prospect over the longer term, even if the growth rate of production will be lower than in the past. For example, in the case of cereals, we should be thinking in terms of world production growing from the 1.8 billion tons of the mid-1990s to about 2.9 billion tons by 2030 (5). Obviously, trade will contribute to spread the associated environmental pressures more evenly across the globe. This raises the issue of how trade and the distribution of environmental pressures over the globe are related. Will trade help assign relatively more pressures to countries that can best respond to them, given their resource endowments and technological prowess? This issue can be addressed schematically with the aid of a simple taxonomy of the combinations of natural resources and technology used in production, on the one hand, and development levels, on the other (examples given in refs. 5 and 18 ). The former determines the extent to which the growth of production enhances the risk of adverse environmental impacts, whereas the latter is instrumental in determining the value people assign to resource conservation and the environment relative to the more conventional benefits from increased production, e.g., food security, farm incomes, and export earnings. Such a taxonomy can help put in a world context the environmental risks of more intensive grain production in the developed exporting countries and make it possible to compare them with those incurred by other countries that would also be raising their grain production. It will also provide useful information for judging the extent to which enhanced production for export in the developed countries may contribute to world food security by making world agriculture as a whole more sustainable, or less unsustainable—if one subscribed to the view that the ever-growing volume of overall economic activity is putting the world on an unsustainable path. This is not the place to develop this subject, but raising the issue is certainly an integral part of any debate concerning world food futures and the role of the different countries.

CONCLUSIONS The fears of impending food crisis that dominated the thinking of some observers up to about mid-1997 have subsided following the reversal of the signals of scarcity (rising prices in world markets). ‡‡ It is now well accepted that, at least over the medium term, there appear to be no major global constraints to expanding world food production at a rate sufficient to match the growth of the effective demand for food (see, for example, ref. 17 ). The deceleration over time of the effective demand for food contributes materially to this “happy” state of affairs. Such deceleration results from both positive and negative developments from the standpoint of human welfare. The positive ones are the slowdown in population growth because of reductions in fertility around the world and the fact that an ever-growing proportion of world population gradually achieves sufficient levels of nutrition beyond which there is only limited scope for further increases in per person food demand. The negative aspects are the contribution of higher mortality (than they would be otherwise—see footnote || ) to the slowing of global population growth, and the role of poverty in depressing demand for food. Demand for food is decelerating because a significant part of world population with still very inadequate consumption levels lacks purchasing power and has no way of expressing the need to increase consumption in the form of solvable demand in the marketplace. This is why the problems of food insecurity afflicting many countries and population groups remain as severe as ever, regardless that price trends in world markets indicate once again an overabundance of food relative to effective demand at the global level. World market prices do not reflect adequately the problems of the poor and the food insecure. Our findings leave no scope for complacency concerning the prospects that progress during the period up to 2010, and perhaps also well beyond it, will be of a pace and pattern such as to eliminate, or significantly reduce, food insecurity. This is a pragmatic and far from optimistic assessment, even if those

‡‡ The latest (mid-December 1998) quote for wheat (U.S. No. 1 H.W., f.o.b. Gulf) is U.S. $126/ton, compared with about U.S. $210/ton in late 1996.

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who think that the world is going to end tomorrow will find unduly optimistic any notion that further progress, slow and uneven as it may be, can be made. The views expressed herein are the author’s and not necessarily those of Food and Agriculture Organization. All data come from Food and Agriculture Organization’s Faostat database ( http://apps.fao.org/cgi-bin/nph-db.pl ), except where otherwise indicated. 1. Food and Agriculture Organization (1996) Food, Agriculture and Food Security: Developments Since the World Food Conference and Prospects,Technical Background Document No. 1 for the World Food Summit (Food and Agriculture Organization , Rome). 2. Brown, L. (1995) Who Will Feed China: Wake-up Call for a Small Planet (Norton , New York). 3. Alexandratos, N. (1996) Agric. Econ. 15, 1–16 4. Alexandratos, N. & de Haen, H. (1995) Food Policy 20, 359–366 . 5. Alexandratos, N. & Bruinsma, J. (1998) in Agriculture and World Trade Liberalisation: Socio-environmental Perspectives on the CAP,eds. Redclift, M. R. , Lekakis, J. & Zanias, G. (CAB , Wallingford, U.K.). 6. Brown, L. (1996) Tough Choices: Facing the Challenge of Food Scarcity (Norton , New York) . 7. World Bank (1997) Commodity Markets and the Developing Countries No. 4 . 8. Johnson, D. G. (1999) Proc. Natl. Acad. Sci. USA 96, 5915–5920 . 9. Food and Agriculture Organization (1996) Assessment of Feasible Progress in Food Security, Technical Background Document No. 14 for the World Food Summit (Food and Agriculture Organization , Rome). 10. Mellor, J. W. , ed. (1995) Agriculture on the Road to Industrialization (Johns Hopkins Univ. Press , Baltimore). 11. Lewis, W. A. (1953) Report on Industrialization and the Gold Coast (Govt. Printing Office , Accra, Gold Coast). 12. United Nations (1996) World Population Prospects: The 1996 Revision (United Nations , New York). 13. World Bank (1998) Global Economic Prospects and the Developing Countries 1998/99: Beyond Financial Crisis (World Bank , Washington, DC). 14. Alexandratos, N. , ed. (1995) World Agriculture: Toward 2010, an FAO Study (Wiley , New York). 15. Alexandratos, N. , ed. (1988) World Agriculture: Toward 2000, an FAO Study (New York Univ. Press , New York). 16. Dyson, T. (1996) Population and Food: Global Trends and Future Prospects (Routledge , London). 17. Ingco, M. , Mitchell, D. & McCalla, A. (1996) Global Food Supply Prospects, World Bank Technical Paper 353 (World Bank , Washington, DC). 18. Food and Agriculture Organization Commodities and Trade Division (1996) Environment, Sustainability and Trade Linkages for Basic Foodstuffs (Food and Agriculture Organization , Rome).

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

The growth of demand will limit output growth for food over the next quarter century

D. GALE JOHNSON * Department of Economics, University of Chicago, 1126 East 59th Street, Chicago, IL 60637 ABSTRACT The rate of growth of world food demand will be much slower for 1990–2010 than it was for the prior three decades. The major factor determining the increase in food demand is population growth. Income growth has a much smaller effect. From 1960 to 1990, population growth accounted for approximately three fourths of the growth in demand or use of grain. For 1990–2010, it is anticipated that population growth will account for nearly all of the increase in world demand for grain. The rate of population growth from 1990 to 2020 is projected to be at an annual rate of 1.3% compared with 1.9% for 1960 to 1990—a decline of more than 30%. World per capita use of grain will increase very little—perhaps by 4%. The increase in grain use is projected to be 40% less than in 1960–1990. It is anticipated that real grain prices will decline during the period, although not nearly as much as the 40% decline in the previous three decades. Concern has been expressed concerning the deterioration of the quality and productivity of the world’s farmland. A study for China and Indonesia indicates that there has been no significant change in the productive capacity of the land over the past 50 years. Contrary to numerous claims, the depth of the topsoil has not changed, indicating that erosion has had little or no impact. The past half century has witnessed an unparalleled improvement in the per capita consumption of food in the world. The improvement has occurred in both the developed and, with the exception of sub-Saharan Africa, developing regions. In the case of sub-Saharan Africa, the failure to achieve a significant increase in per capita food supplies has been due, not primarily to limitations of natural resources, but to wholly inappropriate national policies that exploited agriculture in the name of promoting economic development as well as by ethnic and civil strife in several countries. A World Bank study of the effects of governmental intervention found for 1960–1984 that for three countries in sub-Saharan Africa the returns received by farmers were reduced by 51.6% (1). This meant that farmers received less than half what they would have received had their prices been at the international price levels, with adjustment for local costs of marketing and transportation. The study considered both direct interventions, such as export taxes, and indirect ones, such as overvalued currencies and industrial tariff protection. It was estimated that if farmers had received the international market prices (i.e., the governmental interventions were removed) that output would have increased by 57% (2). This result assumed a period of adjustment of two decades. The three countries were the Ivory Coast, Ghana, and Zambia. The prospectus for this conference noted that world grain production doubled in the last three decades. The doubling of grain production in three decades was a remarkable achievement, without parallel in the history of the world. Such an important accomplishment would seem to merit at least a mild amount of applause. But the next few sentences of the prospectus seem to imply that the doubling has left the world with a great array of problems that will be difficult, if not impossible, to solve. Concern over the impact of population and the spread of agriculture and other forms of human settlements on the environment and the capacity of the world to provide for a growing population is hardly new. This statement is supported by the words of Quintus Septimus Florens Tertullianus, written about A.D. 200: “Indeed it is certain, it is clear to see, that the earth itself is more cultivated and developed than in early times . . . The most charming farms obliterate empty spaces, ploughed fields vanquish forests, sandy places are planted with crops, stones are fixed, swamps are drained, and there are great cities where formerly hardly a hut . . . everywhere there is a dwelling, everywhere a multitude, everywhere a government, everywhere there is life. The greatest evidence of the large number of people: we are burdensome to the world, the resources are scarcely adequate to us and our needs straiten us and complaints are everywhere while already nature does not sustain us. Truly, pestilence and hunger and war and flood must be considered as a remedy for nations, like a pruning back of the human race becoming excessive in numbers.” [translated from Latin by Bart K. Holland (3)]. Whether or not the world is faced with rapid population growth, we do know that the rate of world population growth is now much lower than it was and that prospective rates of population growth are expected to be much less than either recent or current rates. From 1950 to 1990, the annual rate of growth of world population was 1.88%; the annual rate of growth peaked in 1965–1970 at 2.1%. Bos et al. (4) of the World Bank projected that the annual rate of growth of world population for 1995–2000 would be 1.43% and for 2000–2005, 1.24%, and for 2020– 2025, 0.85%—a decline of 60% from the peak rate. Is 1.43% or 1.24% annually a rapid rate of population growth? What about the 1.04% projected for 2015–2020? The rates are not holding constant. They are projected to decline and decline substantially over the next quarter century. At least to me, these are substantial declines and do not represent a rapid growth rate unless any positive rate of growth is so considered. It is quite common to note with alarm that one or more measures of world per capita production or consumption is declining. Let me state categorically: in the world of the past half century, changes in world per capita production or consumption provide little or no useful information. It is possible for world per capita production or consumption of grain to remain constant or to actually decline a little, and

PNAS is available online at www.pnas.org. * To whom reprint requests should be addressed. e-mail: [email protected] .

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yet for every person in the world to be consuming more grain. How can this be? The reason is that there are large differences in per capita food consumption by income levels, and the population weights used to calculate the world per capita averages over time are shifting weights—the low-income consumers with their lower per capita consumption of grain have increased in relative importance in the world’s population. Although the example given is possible, it is only hypothetical. But we do know that from 1979–1981 to 1990–1992 that world per capita grain production increased only from 325 kilograms to 326 kilograms while per capita production in developing countries increased by 7% (14 kilograms) and in developed countries by 2% (14 kilograms) (5). † Concern is expressed that world agricultural output will not grow at as rapid a rate in the future as it did, say, between 1960 and 1990. It is argued that world grain production and world food production as well have grown quite slowly during the 1990s and that world per capita grain production has declined. World grain production has not kept pace with world population growth since 1984. Is this a cause for alarm? As I will argue, it is not. The Rate of Output Growth Is Slowing. Let me state at the outset that the future growth of world grain production and of any other measure of world food supply will be significantly slower than the annual rate of growth during 1960– 1990. This is nearly as certain as it is that the sun will rise tomorrow morning. And it is not a cause for alarm or concern and don’t let any one tell you that it is. Or at least don’t believe them if they do. The reason for the slower growth will be economic rather than the limitations of the biological potential for increasing yields or deterioration in the natural resources used in producing food. Farmers of the world would face disaster if future output grew at the same rate as in the past several decades because if output grew exogenously at that rate, there would be sharply declining real prices. Consequently, output will not grow at the same rate as in the past. But let me hasten to add that the supply of food will grow more rapidly than will demand, real food prices will fall, and per capita food consumption in developing countries will continue to grow at about the same rate as in the past two decades. It will be the growth of demand that will limit the growth of agricultural output over the next quarter century. This is no change from the experience of the last three or four decades of the 20th century. The primary difference is that both demand and output will grow at much slower rates than in the recent past. While grain output increased by nearly 2.5% annually from 1960 to 1990, it did so while the real international prices of grain fell by about 40% (see Table 1). The growth of grain output would have been substantially greater had real grain prices not declined by such a large percentage. In other words, if demand had grown faster so that real grain prices would not have declined, the growth of supply would have been greater than it actually was. There would have been incentives for farmers to produce more by bringing more land under cultivation, increasing the application of chemical inputs per unit of land cultivated, and taking other measures to increase yields that would have been profitable at substantially higher real output prices than they actually received. There would also have been incentives for both governments and the private sector to have invested substantially more in agricultural research and thus have increased output-enhancing innovations and contributed to a higher rate of growth of agricultural output. But the fact was that the growth rate of supply exceeded that of demand for 1960–1990 and real farm prices fell, not by a little but by a lot. The growth rate of demand is not the same as the growth rate of consumption or use. The growth rate of demand measures the shift in the demand function and it would be the same as the growth rate of consumption only if real prices remain unchanged. Put another way, the growth rate of consumption is the result of the shift in the demand function and the change in real prices. From 1960 to 1990, the world’s demand for food grew more slowly than did supply. This is the reason that real international prices of grain declined so very much in the three decades. Had

† The same difficulty in interpreting an average applies among regions in developing countries or even between rural and urban areas in a given country. Whenever there are differences in consumption levels that are correlated with changes in the rates of growth of population, changes in per capita averages will transmit little information and may, in fact, be misleading.

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demand increased at the same rate as supply, real food prices would have remained constant. As I shall show later, the growth of demand for grain (and food generally) will be at a much lower rate than in the recent past. To approximately match the growth of demand, the growth of supply will be much lower than in the past. Recent Trends in World Grain Production. It has been noted that since 1990—or even earlier—world per capita grain production has been declining, and some believe that this is a cause for concern. There are two good reasons why this decline, which has occurred, should not be a matter of significant concern to the populations of the developing countries. As noted earlier, changes in world per capita measures of production or consumption need to be interpreted with extreme caution; per capita grain production tells us almost nothing about the adequacy of food supplies for particular large segments of the world’s population. ‡ As noted, world per capita production of grain was 325 kilograms in 1979–1981 and 326 kilograms in 1990–1992. If per capita production had remained constant in both the developing and developed regions between 1979–1981 and 1990–1992, world per capita production would have declined from 325 kilograms to 312 kilograms—a decline of 4%. When there are divergent regional trends in population growth, world average figures are not reliable measures of what is happening to the production or consumption levels in either the developing or developed countries. The other reason is that the decline in per capita world grain production that has occurred in the 1990s needs careful interpretation concerning its cause and its implications to the large majority of the world’s population—the population of the developing countries. The decline in the rate of growth of world grain production in the 1990s is due primarily to the sharp decline in grain production in Central and Eastern Europe (CEE) during the transition from planned economies to market economies. If grain production in that region had been maintained at the 1985–1989 level rather than declining by more than 100 million tons, the rate of growth of world grain production from 1990 to 1996 would have been at an annual rate of 1.8%, only a little below the rate of 2.1% for the 1980s (7). Did this decline in grain production in the CEEs adversely affect consumption in the rest of the world? The net effect of the transition process on both production and consumption of grain in the CEEs was to increase grain supplies in the rest of the world compared with what it would have been if grain production, utilization, and trade had been maintained at the 1985–1989 levels. This outcome occurred because the consumption of grain in the CEEs decreased more than did production. This was due mainly to two factors. First, the consumption of livestock products was highly subsidized in the U.S.S.R. as well as elsewhere in the region. Consumers in the U.S.S.R. paid less than half of the cost of bringing meat and milk to the grocery store. These subsidies were eliminated after 1991, and the consumption of livestock products was reduced substantially as a result. In addition, real per capita incomes have fallen, reducing the demand for livestock products and, thus, the use of grain as feed. The net effect has been that annual grain imports by the CEEs have fallen by at least 30 million tons, compared with the late 1980s. Consequently, the rest of the world has been able to increase its utilization of grain by 30 million tons as a result of the changes that have occurred in the CEEs. § Again let me emphasize, one must exercise great care in interpreting average changes for the world, such as declining average yields or declining per capita production or consumption. It behooves us to look behind the changes in the world averages and determine what factors were involved before coming to any conclusion concerning the interpretation of the change in the average. Growth of Demand. Demand growth for the next two decades will be at a much lower rate than in the recent past. The growth in the world’s consumption of food is a function of four variables—population, real per capita income, the relative price of food, and differential rates of population growth among countries or regions with different levels of real per capita incomes. Real incomes affect food demand through the income elasticity of demand—a 1% increase in real per capita income increases per capita demand by much less than 1%—in the case of grain perhaps by about 0.10– 0.25%. ¶ As real incomes increase around the world, the income elasticity of demand declines. Food prices at the farm level have a minor effect on per capita food consumption because the farm price represents only a part of the cost to urban consumers, and the price elasticity of demand has become quite low and will be lower in the future than it now is. The primary factor affecting the growth in demand for food is population growth. There seems to be little recognition by those who express concern about future food demand growth of how fast fertility is declining in today’s world and how much further it will decline in the years ahead. Based on data for 1960– 1990, the growth of population accounted for approximately three fourths of the growth in total grain consumption. Increased real per capita incomes and declining grain prices accounted for the remaining quarter of the increase in per capita consumption. Of the 2.46% annual growth in total grain consumption, population growth accounted for 1.9% and per capita consumption growth for 0.55%. What does the future hold? The projections of world population growth by the United Nations and the World Bank imply a sharp fall in prospective growth rates compared with those for the last decades of this century. The projections that I shall refer to are the medium projections, not the high or the low. Two recent projections of the world population for 2020 are 7.67 billion by the United Nations and 7.742 billion by the World Bank. These represent percent increases relative to 1990 of 45.6 and 47.0 respectively. These compare with the actual growth of world population of 77% from 1960 to

‡ The per capita grain consumption in the developing countries has increased at a somewhat higher rate than production because net imports have increased at a faster rate than population. Whereas the developing countries were net importers in both 1980 and 1990, the percent increase in net imports was only moderately greater than the percent increase in population. Net grain imports per capita in 1980 were 18 kilograms and in 1990, 21 kilograms. If net grain imports of developing countries increase to 160 million to 210 million tons as projected in the three studies referred to earlier, per capita grain imports would increase to 28–36 kilograms per capita by 2010 (6). To put this amount in perspective, imports would account for about 12–15% of grain use in the developing countries in 2010. § It is not implied that the 30 million tons annually has gone to importers; some part of it remained in the exporting countries. The only point is that the decline in grain production in the former U.S.S.R. has not imposed a reduction in grain utilization in the rest of the world. ¶ These are rough estimates of the income elasticity of demand, with 0.25 being for the developing countries. An annual growth of real per capita income of 2% would result in annual increases in the per capita consumption of grain of 0.5%. Because of the uncertainties concerning developments in grain production and incomes in the former Soviet Union it is much more difficult to estimate the income elasticity of demand for grain in the developed countries. Pinstrup-Andersen et al. (8) projected a very small increase in world per capita demand for grain from 1993 to 2020—less than 2% for the entire period, but with a significant increase in the per capita consumption of grain in the developing countries.

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1990. || According to the World Bank estimates (4), the growth rate of population is projected to decline by 38%, from an annual rate of growth of 1.9% for 1960–1990 to 1.3% for 1990–2020. In 1994, the three major international organizations with concerns for agriculture, the Food and Agricultural Organization (FAO), the International Food Policy Research Institute (IFPRI), and the World Bank (WB), completed studies of the prospective food demand and supply to 2010. There was remarkable unanimity of results, both with respect to the growth of demand and to supply. The consensus of the three studies was that for the two decades ending in 2010, world per capita consumption of grain would remain approximately constant, but would increase in both developing and developed countries by small percentages (9). According to these studies, the world consumption of grain is and will be moved almost entirely by population growth. At the time the studies were being prepared, the projection of the annual rate of world population growth for 1990–2010 was 1.5%. Their consensus estimate was that world consumption of grain would grow at approximately 1.5–1.7% annually, which was consistent with their conclusion that the weighted average of world per capita consumption would increase very little. Extending the consensus projection of the three studies for 1990–2010 to the year 2020, I project that the production of grain will increase by 17% in the developing countries in 2020 and by 9% in the developed countries. This would increase per capita production to 250 kilograms in developing countries and to 750 kilograms in the developed countries. In 2020, it is projected that the developing countries will have 82.2% of the world’s population, up from 77% in 1990. World per capita production in 2020 would be 339 kilograms [(0.178 × 750) + (0.822 × 250) = 339]. ** This is an increase of 4% from the 1990 world per capita production. In terms of annual growth, the projected growth in world utilization of grain would be very slightly more than 1.3% annually—the projected rate of growth of population plus a 4% increase in per capita use. Enough Food to Eliminate Malnutrition? There are many people in the world who are chronically undernourished. As of 1988–1990, 781 million were estimated to be chronically undernourished. The indicated projection of demand assumes that the number will decline to 637 million in 2010 and to about 575 million in 2020. The primary factor responsible for malnutrition is low income levels rather than an inadequate supply of food. Low levels of caloric intake are not the sole cause of malnutrition and perhaps not even the major cause. Deficiencies in the availability of micronutrients such as vitamins A and D, iron, iodine, and calcium, plus the heavy incidence of dysentery in many low income areas of the world, contribute to the problem. The Food and Agricultural Organization (10) has estimated that to increase the dietary energy supply to 2,300 kcal (1 kcal = 4.18 J) per day in 2010 of the countries that had a supply of less than 1,850 kcal/day in 1990 would require 46 million tons of grain. This assumes that grain supplies 60% of the energy supply and would do so in 2010. The addition to the supply of grain for the developing countries that in 1990 had per capita daily energy supplies of less than 1,850 kcal/day would be 8.5% of the projected supply in 2010, but only 2.4% of projected world grain production. It would require a rather modest increase in the price of grain (almost certainly no more than 10%) to achieve such an increase in world grain production. But even if all of the increase in calories had to come from grain, the required increase in grain would be about 75 million tons, or less than 4% of current world grain production, and approximately 2.5% of projected world production in 2020. Recent Price Trends. Table 1 gives data on the real prices of wheat, rice, and corn for the period since 1950. These are based on U.S. export prices for wheat and corn and Thailand’s export prices for rice, and the deflator is the U.S. wholesale price index. †† During the 1990s, the international prices of grain have been nearly the lowest that they have been in the 20th century. This is in spite of the temporary run-up in prices in the mid-1990s. The price increases in 1995 and 1996 have now been largely erased, and the real export prices in 1997 had almost returned to the low levels of 1990–1994. This year, China introduced a price support program to raise the low market prices of grain that farmers were receiving. China is not now a significant importer of grain, in spite of wild and unsupported projections that it would be. China did import significant amounts of grain— nearly 20 million tons—in 1995 but this was done in error; China had a bumper grain crop in 1995 as it did in 1996 and had no need for imports. China now faces the problem of large stocks and low domestic prices of grain. It exported an average of 5 million tons of grain in 1992, 1993, and 1994 (11), in contrast to its position as a net importer of 13 million tons a decade earlier (1980–1983) (12). President Clinton visited China, and not long after returning, he also announced that the price of wheat was too low. He authorized the purchase by the U.S. government of 80 million bushels of wheat, which will be used for food aid and thus (largely) removed from the domestic and world market. It is estimated that this action will increase the market price of wheat by 10 to 13 cents per bushel. It is quite remarkable that politicians in the world’s two largest grain-producing countries should simultaneously decide that so much grain had been produced that it was necessary to take action to increase grain prices. True, a factor in the current low prices of grain is the economic slowdown in several Asian countries combined with a delayed output response by farmers to the relatively high real prices of 1995 and 1996. However, the current international market prices of grain are not significantly below those that prevailed in 1990–1994.

|| The medium projections may well be on the high side for years some distance in the future. The reason is that in the two projections noted in the text, the demographers who make the projections must decide what to assume for the countries that now have fertility rates below replacement level. They resolved this issue by assuming that fertility will actually increase to the replacement level in the not too distant future. For example, Germany is assumed to increase its fertility level to 2.1 (actually 2.076) by 2035 compared with its recent level of 1.3 (4). China is thought to have a fertility rate of 1.9 in 1995–2000 and this is projected to increase to 2.127 in 2025–2030. I report this aspect of the two projections to make it clear that the projected levels of population do not assume that countries that have fertility below replacement levels will continue to follow the path of recent trends. Quite the contrary, it is assumed that in these countries fertility will increase over the next three decades or so and in some cases by significant percentages. So far as I know, there is no foundation for this assumption but some assumption had to be made to complete the projections. ** Per capita utilization of grain would differ somewhat from per capita production because of projected imports of grain by the developing countries. In 1990, developing countries imported 21.5 kilograms of grain per capita and they are projected to import 28–36 kilograms in 2010. If developing country imports continue to grow between 2010 and 2020 at approximately the same rate as from 1990 to 2010, then per capita consumption might be 285–290 kilograms. Given the shift in population weights, the increase in world per capita utilization would be a little less than 4%. †† I have used the U.S. wholesale price index rather than the World Bank’s index of the prices of manufactured products exported by the industrial countries to the developing countries. Over time that index increases much more than the U.S. wholesale price index and if it is used as a deflator, the declines in the real prices of grains are much greater than what is reflected in Table 1 . For example, if the World Bank’s index is used, the real international price of corn declined by 48% between 1950 and 1990. In Table 1 , the decline is 37%. The U.S. wholesale price index has a much broader commodity coverage than the World Bank index. The U.S. index includes oil and coal, for example.

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Not all of the implications of the current low grain prices are positive. The low prices do not encourage governments to take the long-term view with respect to investment in agricultural research or changing policies that adversely affect farm output. It is possible that if these low prices continue for another year or two, as they might well do, world grain production will stop expanding and grain stocks will decline, resulting in another price spike such as occurred in 1995 and 1996. This will not presage a significant decline in the long run growth of grain output, but price instability imposes costs on both farmers and consumers. Will Cropland Area Increase? It may be noted that in the studies of future food supplies that I have used, there is an implicit assumption that the area devoted to grain will increase little, if at all, in the years ahead. True, there has been little increase in recent years. In fact, the grain area harvested in 1996 was the same as in 1970 (7). But why should there have been an increase in harvested area? It was cheaper to find substitutes for land than it was to increase the area of land devoted to grain. With the rapid rate of decline of the real price of grain, there was little incentive to pay the substantial cost of increasing the cropland area even though there is widespread agreement, even including the Club of Rome, that the amount of arable land in the world could be increased by 50% (13). I think it is unlikely that over the next two decades there will be any significant increase in the cropland area, but there could be if agricultural prices increased significantly. But higher real prices for farm products are highly unlikely, so it is unlikely that we will see the development of much new cropland. A failure to increase cropland will be a signal that yield increases on existing cropland have been sufficient to meet the slow growth in demand that will occur. Two Possible Threats to Future Food Supply. The increase in irrigated area since 1950 has been an important factor in the higher yields of grain and other agricultural products. It is argued that it is unlikely that there will be a significant increase in irrigated area in the near future and that it is possible that the irrigated area could decline because of depletion of existing supplies of stored water, of larger withdrawals from aquifers than the rate of replacement, or of increased use of limited water supplies by nonagricultural activities. These outcomes cannot be ruled out. No country in the world properly manages its water supply. Almost everywhere, water is a commonproperty resource and no value is attached to the water at the source, whether from an aquifer or from a storage facility such as a lake or a reservoir (14). At most, farmers are charged for the cost of delivering the water to the field. Several countries actually subsidize the delivery of water to urban consumers and for irrigation. A large percentage of the existing irrigated water is wasted, and there is a substantial potential for saving water with little effect on output; the way water is generally priced, the individual farmer has little incentive to economize in its use. A common practice is to provide a farmer with a particular volume of water at a fixed price. The farmer gains nothing by using less than the fixed volume of water. Or if water is being pumped from an aquifer, there is seldom a limit to the amount of water that can be withdrawn, and there is no charge for the value of the water in the aquifer. Often, as is true in India, the electricity used to pump the water is heavily subsidized: in the Punjab, the electricity used in pumping water for irrigation is free. Until governments recognize that water is a valuable resource and price it properly, there is reason to be concerned that the savings in irrigation water will not come soon enough to prevent some irrigated areas from being abandoned because they have exhausted their available supply of water or they have been forced to give up their water for a higher value use. Irrigated areas may also be lost to salinization and waterlogging, but at a cost these can be corrected. Another common property resource that is important to the world’s food supply is that of ocean fisheries. Here the misuse of the world’s resource is similar to that for irrigation water. Outside the 200-mile limit, there is no significant effort to limit the amount of fish taken—access to the commons is not limited. The amount now being taken exceeds current annual growth, and the breeding stocks of several important fish species are in serious danger of depletion. One important reason for the depletion of ocean fisheries has been the technological changes in the methods of catching fish that have occurred in the past three or four decades. Another reason is that many governments subsidize their fishing industry. Water and ocean fishing are two areas where major problems affecting the world’s food supply either exist or potentially may do so. In both cases it takes action by governments to find appropriate solutions. Although markets could be part or all of the solution, markets for common-property resources cannot exist without government(s) creating the necessary framework by assigning property rights or by using markets to privatize the rights. In one way or another, governments must find ways of restricting access to common-property resources. In the case of water, each government is largely in control of its own destiny, although there are numerous examples of where a common water source is shared among two or more countries. In the case of ocean fisheries, agreement is required among many governments if the world’s fisheries are not to be seriously depleted. If governments are either unable or unwilling to find solutions for the common property problem that falls entirely in their own jurisdiction, it may be unrealistic to assume that they can find solutions for a common property problem that requires agreement among scores of governments until the catch from ocean fisheries is substantially lower than the current level and fish prices are much higher than they are now. Unfortunately, fish farming has offset the loss of catch from the oceans and thus permits governments to delay seriously tackling the issue. I say it is unfortunate because there is no feed cost to fish taken from the ocean; the only cost is catching them. But most farm-raised fish require feed and in significant amounts. By not solving the ocean fishing problem, a source of food that directly competes with neither humans nor domestic animals is lost. Has the World’s Cropland Been Seriously Degraded? It is alleged that the quality of the world’s land resource has been degraded through erosion, loss of organic matter, and other forms of loss of potential productive power. ‡‡ There are claims that enormous quantities of topsoil are lost each year to water and wind erosion. Does the world enter the next millennium with soil that is badly degraded and of lower productive capacity than it was when we entered the 20th century or in 1950 when the recent surge in agricultural productivity started? There are many allegations that this is the case. Such allegations emanate from the Worldwatch Institute and the World Resources Institute, for example. Some aspects of these claims were endorsed by the presidents of the Chinese and the United States academies of sciences in a statement issued in Beijing on January 16, 1997. They agreed that “The need for improvement is urgent, since all resource indicators— changes in the atmosphere, loss of topsoil, loss of forests, the extinction of organisms—have moved sharply and continuously downward during the second half of the 20th century, while both world population and levels of consumption continue to rise. Globally, these trends are not sustainable over the long run.” Among the impending disasters, I shall consider only the loss of topsoil from agricultural lands.

‡‡ Erosion occurred long before man was a factor in affecting the world’s environment. And not all erosion has adverse effects on the productivity of the land. An example is the southwestern part of the state of my birth, Iowa. This part of Iowa has some of the deepest topsoil in the world, and much of it was created by erosion; it was transported by wind from Texas and Oklahoma. The soil is much more productive where it now is than if the erosion had not occurred.

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I agree with Peter H. Lindert (15, 16) of the University of California at Davis that the claims that there have been serious loss of topsoil from agricultural lands or other forms of widespread deterioration of the productive capacity of farm land are without foundation, i.e., not based on evidence of change over time. Lindert (16) states the following: “Lacking an actual quantitative history of soil conditions beyond experimental plots, scholars have fixed on the useful but risky task summarized by the title of this section. §§ The literature has three main shortcomings: (1) using crude indicators that prove little about human impacts on the soils, (2) using trends in cultivated land area as clues about land quality, and (3) using single-snapshot predictions as if they were time-series data.” ¶¶ Lindert used long-run data from two large developing countries, China and Indonesia, in an effort to measure changes in the quality of the land resource. The data he used were soil surveys, dating from the 1930s to the relatively recent past, the 1980s in China and 1990 in Indonesia. This is not the place to provide a detailed summary of his results, but his following brief summary will provide a sharply different perspective than those that are commonly given (16). “The broadest outlines of the interaction of soil and agriculture are now somewhat clearer for two developing countries. We have some idea which dimensions of soil quality have improved and which have not. Soil organic matter and nitrogen appear to have declined on cultivated lands in both China and Indonesia. Total phosphorous and potassium have generally risen. Alkalinity and acidity have fluctuated, with no over overall worsening. The topsoil layer has not gotten thinner. “Some of the mixed trends revealed here have more effects on yields than others. China’s patterns show that the decline in soil organic matter and nitrogen makes little difference, presumably because fertilizers can substitute for the soil endowment. More relevant are the pH and total potassium, for which the trends are better.” Based on comparisons of soil surveys over a period of 50 years, Lindert (16) reaches the remarkable conclusion for China and Indonesia: “The topsoil layer has not gotten thinner.” This conclusion is wholly inconsistent with the statements from the presidents of the two academies of science and from most other commentators on the subject. This is not to deny that erosion exists in China, after all, the Yellow River didn’t get its name by accident. But to note that there are obvious signs of erosion does not tell us from whence it came or why it occurred. The data assembled by Lindert indicates that it has not come to any considerable extent from farmland. I find it hard to believe that farmers are as careless with a resource that is very important to them as is implied by much of the opinion expressed concerning the alleged enormous loss of topsoil. I have long held that farmers are at least as smart as the rest of us and I believe that they know how to act in their own interest. It is not in the interest of farmers to prevent all erosion because there are likely to be costs involved. But in the range where the benefits and costs of preventing erosion are approximately equal or the benefits exceed the costs, it seems reasonable to assume that farmers are acting in their own interest, at least until there is solid evidence to the contrary. Lindert’s analysis of historical data for two important countries indicate that there may not be evidence to the contrary. Soil surveys do exist in other countries. It is perhaps time that more use is made of this neglected source of information about the state of the world’s land resource and less reliance is placed on information that lacks a time dimension. Concluding Comments. The people of the world are better fed than ever before. And more people will have more adequate nutrition 20 years from now if the governments of the world carry out their responsibilities with the same care and intelligence as farmers display in their production activities. In my opinion, an important danger to the future of the adequacy of the world’s food supply are low international prices, given the responses governments of both developed and developing countries are likely to make. In the face of current low international prices for grain, will governments maintain their investment in agricultural research? The declining real support for agricultural research in the past decade or so has been to some degree a response to low prices. If there are to be continuing improvements in the adequacy of food supplies in developing countries, the support of agricultural research must not be reduced and probably should be increased. A second danger is that there are still developing countries that are following policies that discriminate against agriculture and farm people. As long as these policies persist, the growth of food production will lag and people will unnecessarily suffer from malnutrition. A large percentage of the malnourished people in the developing countries live in rural areas and depend on agriculture for all or most of their incomes. For these people there is a close link between farm prices, food output growth, incomes, and their nutritional status. Financial assistance from the William ImMasche Foundation is gratefully acknowledged. I alone am responsible for the content of the paper. 1. Kreuger, A. O. , Schiff, M. & Valdes, A. (1991) The Political Economy of Agricultural Pricing Policy (Johns Hopkins Univ. Press , Baltimore), Vol. 3. 2. Schiff, M. & Valdes, A. (1992) The Political Economy of Agricultural Pricing Policy (Johns Hopkins Univ. Press , Baltimore), Vol. 4 . 3. Holland, B. K. (1993) Popul. Dev. Rev. 19, 328–329 . 4. Bos, E. , Vu, M. T. , Massiah, M. & Bulatao, R. A. (1994) World Population Projections: Estimates and Projections with Related Demographic Statistics(Johns Hopkins Univ. Press , Baltimore). 5. Alexandratos, N. (1994) in Population and Food in the Early Twenty-First Century: Meeting Future Food Demand of an Increasing Population,ed. Islam, N. (International Food Policy Research Institute , Washington, DC), pp. 25–48 . 6. Mitchell, D. O. & Ingco, M. D. (1994) in Population and Food in the Early Twenty-First Century: Meeting Future Food Demand of an Increasing Population, ed. Islam, N. (International Food Policy Research Institute , Washington, DC), pp. 49–60 . 7. Food and Agricultural Organization (1997) Production Yearbook (Food and Agricultural Organization , Rome). 8. Pinstrup-Andersen, P. , Pandya-Lorch, R. & Rosegrant, M. W. (1997) The World Food Situation: Recent Developments, Emerging Issues, and LongTerm Prospects(International Food Policy Research Institute , Washington, DC). 9. Islam, N. , ed. (1994) Population and Food in the Early Twenty-First Century: Meeting Future Food Demand of an Increasing Population (International Food Policy Research Institute , Washington, DC), pp. 85–89 . 10. Food and Agricultural Organization (1996) World Food Summit: Technical Background Documents 12–15 (Food and Agricultural Organization , Rome), Vol. 3 , Document 14 , p. 9 . 11. China State Statistical Bureau (1994) China Statistical Yearbook (China Statistical Publishing House , Beijing). 12. China State Statistical Bureau (1984) China Statistical Yearbook (China Statistical Publishing House , Beijing). 13. Oram, P.A. & Hojjati, B. (1994) in Population and Food in the Early Twenty-First Century: Meeting Future Food Demand of an Increasing Population, ed. Islam, N. (International Food Policy Research Institute , Washington, DC), pp. 167–189 . 14. Rosegrant, M. W. (1997) Food, Agriculture, and the Environment Discussion (International Food Policy Research Institute , Washington, DC), Paper 20 . 15. Lindert, P. H. (1996) Soil Degradation and Agricultural Change in Two Developing Countries,Working Paper Series No. 82 (Univ. of California Agricultural History Center , Davis, CA). 16. Lindert, P. H. (1999) Economic Development and Cultural Change 47, in press .

§§

The title of the section was “Judging Soil Quality Trends Without Measuring Them?” Lindert (14) adds the following: “Most importantly, the proffered data on soil quality trends are neither data nor trends. Rather they are experts’ predictions from a single snapshot, derived by combining data on slope, climate, and land use with what happens to such soils under experimental conditions. Sometimes it is refined into ”expert opinion,“ as in the GLASOD map, but it is still not based on any observation before the mid-1980s. That it is not a real history does matter, since the complexity of human soil interventions over a large countryside can defy simulation on experimental plots. Farm populations react to the soil itself with complex mixtures of crop rotations, amendments, fertilizer application, investments in water control, and sometimes neglect and mismanagement. To know the soil impact of recent human interventions, we need data on actual practice over long time spans and large areas.” ¶¶

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This paper was presented at the National Academy of Sciences Colloquium “Plants and Population: Is There Time?” held December 5–6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Global and local implications of biotechnology and climate change for future food supplies

ROBERT E. EVENSON * Department of Economics, Yale University, New Haven, CT 06520 ABSTRACT The development of improved technology for agricultural production and its diffusion to farmers is a process requiring investment and time. A large number of studies of this process have been undertaken. The findings of these studies have been incorporated into a quantitative policy model projecting supplies of commodities (in terms of area and crop yields), equilibrium prices, and international trade volumes to the year 2020. These projections show that a “global food crisis,” as would be manifested in high commodity prices, is unlikely to occur. The same projections show, however, that in many countries, “local food crisis,” as manifested in low agricultural incomes and associated low food consumption in the presence of low food prices, will occur. Simulations show that delays in the diffusion of modern biotechnology research capabilities to developing countries will exacerbate local food crises. Similarly, global climate change will also exacerbate these crises, accentuating the importance of bringing strengthened research capabilities to developing countries.

I. INTRODUCTION Projections of food supply have typically been based on past experience. Economists usually emphasize the continuity and “momentum” of the development and diffusion of improved technology in making these projections. Biological scientists, on the other hand, usually place more stress on the inherent “limits” to supply growth as reflected in “carrying capacity” models. In this paper, food supply projections are based on projections of investments in productivity improvement activities and on evidence regarding the effectiveness of these activities. These projections are incorporated into a global agricultural general equilibrium model [the International Food Policy Research Institute (IFPRI)–International Model for Policy Analysis of Agricultural Commodities (IMPACT) model], which does consider limiting factors to supply growth. These projections are first developed for a “base case,” where they may be compared with other projections. The development of new techniques for developing biological inventions (biotechnology) must be incorporated into the base case, because these techniques are already producing significant inventions. Experience to date with biotechnology, however, is still too limited to be used for projections. A recently completed study of rice biotechnology elicited subjective probability estimates of research potential and of time to achievement of research potential for a large number of research problem areas for rice. This study provides a basis for both the base case projections and for an important policy simulation dealing with the diffusion of biotechnology to developing countries. This paper also introduces a policy simulation for the effects of global climate change based on three recent studies of climate change impacts on agriculture in the United States, India, and Brazil. Although these three studies do not provide comprehensive coverage of global food production, the three studies do fit into a common global pattern showing that cooler regions of the world will benefit from global warming, whereas warmer regions will suffer losses. Not surprisingly, the base case and policy simulations show that “local” effects can differ drastically from “global” effects. The base case computations yield relatively favorable global effects. A “global food crisis” appears not to be in the offing in the next 25 years or so. But that does not mean that “local food crisis” will not continue to exist in 2020. The base case projections show general improvement in local indexes of malnutrition, but even under the most favorable simulations, malnutrition will continue to be a real problem for much of the developing world. The policy simulations show that delays in the diffusion of biotechnology to developing countries is likely to exacerbate local effects. Global warming scenarios also show a worsening of many local effects. The IFPRI-IMPACT model computes price projections that are essentially global. It also computes production, cropped area, and trade projections that are local (i.e., national). The cropped area effects have important implications for biodiversity because, as cropped area expands, biodiversity habitats are altered. Finally, the model also computes measures of child malnutrition based on food consumption projections. Part II of the paper provides a brief overview of the IFPRI–IMPACT model. Part III develops the nonprice supply components of the model. Part IV develops policy scenarios to address the questions noted above. In part V, scenario calculations are reported. Part VI concludes.

II. THE IFPRI–IMPACT MODEL In this section, the IMPACT model is briefly described. The Appendix provides more detail. The IMPACT model developed at IFPRI is a computable equilibrium market model for agricultural products (crops and livestock; 17 commodities). It is based on 35 country–region submodels † . Each submodel consists of equations depicting the supply for each commodity as a function of price and nonprice terms. The demand for each commodity is also

*

To whom reprint requests should be addressed at: 27 Hillhouse, Yale University, New Haven, CT 06520. e-mail: [email protected] . Agcaoili, M. C., Oga, K. & Rosegrant, M. W. (1993) Structure and Operation of the International Food Policy and Trade Simulation (IFPTSIM) Model. Paper presented at the Second Workshop of the Research Project on Projections and Policy Implications of Medium-and Long-Term Rice Supply and Demand [International Rice Research Institute (IRRI), Los Banos, Philippines]. PNAS is available online at www.pnas.org. Abbreviations: IFPRI, International Food Policy Research Institute; IMPACT, International Model for Policy Analysis of Agricultural Commodities; R&D, research and development; ITI, industrial technology infrastructure; NARs, National Agricultural Research systems; IARCs, International Agricultural Research Centers. †

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described as a function of price, income, population, and nonprice terms. The submodels are linked through trade, which may be free or restricted by tariffs. The model solves for global and submodel equilibrium prices for each commodity where all markets are cleared. Linkages with other sectors are built into the model, but these are not sufficiently complex to describe the model as a global general equilibrium model. It is an agricultural general equilibrium model. The endogenous variables determined by the model equilibrium are: 1. Commodity prices and quantities by country–region. 2. Trade quantities (imports and exports) by country– region. 3. Cropped area by commodity by country–region. 4. Commodities consumed; calories per capita; percent children malnourished by country–region. The model also generates the per capita calorie availability from food consumed by using standard kilocalorie conversion values for different foods. Estimates of the relationship between the percentage of children ages 0–6 years malnourished as a function of calorie availability are made from pooled cross-section, time and series data for 61 developing countries for 1980, 1985, and 1990. ‡ The exogenous variables in the model are: 1. Population by year, by country–region. 2. Nonagricultural income by year, by country–region (agricultural incomes are endogenous). 3. Total land area by country–region. 4. Nonprice (productivity) supply growth including contributions from: a. Farmers’ schooling b. Agricultural extension c. Public-sector agricultural research d. Private-sector agricultural research. Population and income projections are taken from World Population Prospects (1). Irrigation projections are based on IFPRI studies. Nonagricultural income projections are based on World Bank and Asian Development Bank sources. Price and income elasticities of demand are taken from national sources where feasible. Harvested area is a function of price (price response parameters are taken from national studies), † total land area, and nonprice factors. Similarly, yields are a function of both price and nonprice factors. Supply is area times yield. Supply elasticities are generally low. A dynamic adjustment process is allowed, consistent with estimates of supply responses in China, India, Indonesia, and other countries. The structure of the model allows for baseline projections to be specified for the exogenous variables. This produces baseline projections for the endogenous variables. Alternative policy scenarios can be defined and projections obtained. These can be compared with the baseline projections.

III. SPECIFYING THE NONPRICE SUPPLY (AREA AND YIELD) TERMS The nonprice supply component for both area and yield is specified as an annual rate of change. This trend can be interpreted as a total factor productivity growth trend. Productivity growth is traceable to several sources. These include improvements in the human capital (schooling) of farmers, agricultural extension programs, and agricultural research programs (public and private), all of which produce positive productivity gains. Resource degradation produces negative productivity gains. The IFPRI–IMPACT model is not based on trend estimates or judgements except to achieve continuity with the recent past. It relies instead on a combination of a detailed ex ante research contribution study for rice production and an extensive body of ex post productivity decomposition studies. Non-price supply trends are developed for both yield and area for 5-yr periods: 1995–2000, 2000–2005, 2005–2010, 2010–2015, and 2015–2020. The starting point for developing these nonprice trends was to examine past nonprice trends in yield and area growth. This was done by first removing price effects from yield and area data and estimating nonprice trends for each commodity and country for the 1962–1982 and 1983–1992 periods. In most cases, these trends were higher in the 1962–1982 “Green Revolution” period. Part of this slowdown is because of a relative exhaustion of “Green Revolution” gains, a fact that is taken into account in the component analysis. Thus, the projected future trends explicitly account for the slowdown in yield growth for most commodities in most countries (as well as accounting for strong performers, such as rice yield growth in India and pork meat and poultry production in much of Asia). For the few countries where base or end-of-year values resulted in trend estimates that were clearly outliers from trends over the 1983–1992 period, these estimates were modified to be consistent with nonoutlier trends. Phase-in rules were used to link these past trends with projected trends. The first step in making nonprice yield projections was to break the projection into its components and subcomponents. The following component structure, based on a study of Indian crop productivity, § ¶ was used: 1. Public [International Agricultural Research Centers (IARC)-National Agricultural Research systems (NARs)] research a. Management research b. Conventional plant breeding c. Widecrossing-hybridization breeding d. Biotechnology (transgenic) breeding 2. Private-sector agriculturally related research and development (R&D) 3. Agricultural extension—farmers’ schooling 4. Markets 5. Infrastructure 6. Irrigation (interacting with technology) The yield growth contribution of modern inputs such as fertilizers is accounted for in price effects in the yield response function and as a complementary input with irrigation and with the modern varieties generated by research. The public sector research subcomponents are based on a rice research priority setting study (2). A. The Public Research Component of Rice. A recently completed study, Rice Research in Asia: Progress and Priorities (2), || provided the basis for subcomponent projections for four broad rice-producing zones (South Asia, Southeast Asia, East Asia, and the rest of the world). The priorities study contributed estimates of crop losses from insect pests, plant diseases, and abiotic stresses for Eastern and Southern India, Indonesia, Bangladesh, Thailand, and China. These crop-loss estimates were treated as estimates of potential gains for specific types

‡

World Nutrition Database ACC-SCN, 1992. This accounting framework allows for productivity contributions from many sources. A number of studies have addressed the contribution of each source. ¶ Rosegrant, M. W. & Evenson, R. E. (1993) Determinants of Productivity Growth in Asian Agriculture: Past and Future. Paper presented at the 1993 American Agricultural Economics Association International Pre-Conference on “Post-Green Revolution Agricultural Development Strategies in the Third World: What Next,” Orlando, Florida. || Evenson, R. E. (1998) “Biotechnology Research Priorities for Rice,” International Rice Research Institute (mimeograph). §

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of research. Insect reduction potentials were based on losses from 13 major insect pests. Disease reduction potentials were based on losses for 14 major rice diseases. Abiotic stress potentials were based on losses (adjusted for the proportion that can be affected by research) for nine abiotic stresses (heat, cold, drought, flooding, etc.). Management potentials were based on data for managementrelated pest problems (weeds, rodents, birds). Biological efficiency potential estimates were based on scientists’ estimates of gains from improved plant design, improved photosynthesis efficiency, shorter growth duration, and improved grain quality. A scientist’s rating exercise was carried out with 18 senior rice scientists in 1995 and followed up in 1997 with a second rating study with an additional 60 scientists. For each of the research problem areas for which respondents had scientific qualifications, four ratings were elicited (ratings were on a scale of 1 to 5 but were calibrated to percentage achievements of economic potential) for alternative research techniques (managerial research, conventional breeding, widecrossing and hybridization, and biotechnology/ transgenic rice and marker-aided selection). These ratings were: 1. A rating of achievement to date (RA); 2. A rating of potential achievement (RP); 3. An estimate of the number of years required to achieve 25% of the difference between achievement to date and potential (Y25); 4. An estimate of the number of years required to achieve 75% of the difference between achievement to date and potential (Y75). In developing these estimates, scientists were asked to presume that both IARC and NARs programs would continue to be supported at the levels of the past decade in future periods. The specification of two ratings, one for achievement to date and one for potential achievement, forced respondents to focus on “remaining potential.” Ratings of potential minus achievements to date were summarized and converted to percent of accomplishments. Estimates were obtained for each research problem area by research technique. For purposes of developing projections, the ratings were scaled into period estimates based on the Y75 estimates. Conventional breeding programs were considered the core genetic (improvement) programs. Widecrossing and marker-aided breeding programs were not expected to contribute to productivity gains until their actual potential achieved exceeded that of conventional breeding. Similarly, transgenic breeding was not projected to contribute to productivity until it exceeded the potential of widecrossing and marker-aided breeding. By converting the ratings to actual percentages and multiplying them times the units affected (crop losses or yield potential), rice nonprice yield projections were created for each region for the public NARs and IARC components. Note that one can distinguish between biotechnology and conventional breeding components, thus enabling the biotechnology slowdown policy scenarios noted below. B. Extension—Schooling Components. Several studies of agricultural extension and schooling have been undertaken (3). It is difficult to generalize as to the growth contribution of extension and schooling, however, because to produce growth, investments must be made and investments must be productive. The most comprehensive study of growth experience to date is the IFPRI study of India (4). That study indicated that the extension contribution was roughly two-thirds of the public research contribution. The management research contribution is also related to the extension contribution. The rule for computing the extension contribution is that extension plus management research is two-thirds of conventional breeding, widecrossing, and biotechnology research. C. The Private-Sector R&D Contribution. The private-sector R&D contribution depends on the stage of industrial technology infrastructure (ITI). The stages range from little or no ITI (stage 1A) to the Newly Industrialized Country type ITI (stage 2C) and developed country ITI (stage D). A study by Evenson and Westphal (5) defines stages for different countries (see Appendix ). Projections of these stages are based on the expectation of the continuation of industrial reforms underway for the past decade. The Appendix summarizes projections of ITI by country, by period. The India growth accounting study (4) indicated approximately a 0.1% growth contribution for India from private-sector R&D. India is a 2A country moving toward 2B status. U.S. evidence suggests a 0.2% contribution (6) for developed countries. Based on these studies, the following private R&D growth components by ITI class were assigned: 1B = 0; 1C = .05; 2A = .1; 2B = .15; 2C = .2; D = .2. D. Markets and Infrastructure Contributions. As with private-sector R&D, these contributions are tied to ITI class. Based on the India study (4), the following markets– infrastructure growth components by ITI class were assigned: 1B = .1; 1C = .1; 2A = .15; 2B = .15; 2C = .2; D = .1. E. Extension to Other Commodities. Scientist ratings are not available for other crops to allow estimates similar to those for rice. However, there is a larger body of evidence from returns to research studies. From this evidence, it appears that research programs have been effective in all cereal grains. Public-sector research has also been effective in oilseed crops (soybeans). It appears that research progress has been slower in rootcrops than for cereals (the Appendix provides further detail on returns to research). The management and conventional breeding components for other commodities have been scaled to the rice estimates by using relative rates of return. F. Nonprice Area Projections. Procedures for estimating nonprice area growth for 1990–1995 followed the same procedures described above for yield. In later time periods, nonprice area components depend on the availability of cultivable land, irrigation, and infrastructure investments and productivity gains as well as prices. Some of the effects operate through prices, and to the extent that they do, the price response parameters within IMPACT, the IFPRI multicommodity model, will determine changes in area. But to the extent that investments expand the effective stock of land, they are nonprice components. In practice, aggregate land expansion has slowed to very low rates in recent years as the stock of cultivable land has been exhausted. The chief component of aggregate area expansion has been investment in irrigation, which has also slowed dramatically in recent years (7). Projections of area expansion in subsequent time periods thus take estimated nonprice area growth trends estimated for 1990– 1995 and in most cases dampen these to reflect the lagged effects of declining investments in irrigation. Accordingly, except for a few crops in a few regions, low rates of nonprice area expansion are projected. Nonprice growth in livestock numbers is projected based on recent historical growth and rates of change in this growth rate from previous periods. Data on rates of return to agricultural research were used to scale the nonprice yield and area parameters for other crops to the rice cases (see Appendix ).

IV. POLICY SCENARIOS The baseline case in the IFPRI–IMPACT model is based on continued support of research and extension programs at present levels. Biotechnology contributions are expected to come on line first for rice then for other commodities, accord-

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ing to scientists. Industrialization and trade liberalization are expected to continue. The following alternative policy scenarios are considered: A. Demographic gift B. Delayed industrialization C. Reduced IARC–NARs support D. A 10-year biotechnology delay E. Climate change A. Demographic Gift. The base case population scenario is based on the U.N. “medium” population projection. The demographic gift projection reduces this to the U.N. “low” projection. This is consistent with the demographic gift (8) associated with reduced population growth. The labor force growth contributing to production will not be reduced until after the time lag between birth and labor force entry occurs. Thus, in the period from 1990 (1998) to 2020, labor force will grow at the medium projection, but the number of prelabor force consumers will decline. This is a one-time “gift” in the sense that the ratio of laborers to population will rise only for a short period before it returns to normal as labor force growth slows. B. Delayed Industrialization. Another realistic scenario is that of delayed industrialization reforms. The past 10–15 years have seen considerable progress by a substantial number of developing economies in improving trade and industrialization policy. This has enabled many countries to move forward in the ITI classification. Indonesia, for example, has moved from a 1C technological infrastructure level to 2A and now to 2B. Continued reform to 2C status is postulated in the base case. Similarly, Thailand has moved from 2A to 2C over the past two decades, while the Philippines has remained at the 2A level. Latin American countries have generally made improvements as well. But this move toward industrialization and the rapid growth associated with it can be reversed and delayed. This may come about because of increased local conflicts (by and large, countries with significant civil strife do not make economic progress). The recent crisis in Asia demonstrates this effectively. This scenario is one where the ITI class standings for 1995–2000 are maintained through subsequent periods. A more severe industrialization delay would call for a reversal of some of the recently attained standings (for example, political turmoil in Indonesia could cause a reversion to 2A or even IC status). C. Reduced IARC–NARs Support. A substantial shift in international support in terms of loans or grants for NARs and IARCs over recent decades has taken place. In the 1950s, 1960s, and 1970s, bilateral aid agencies supported NARs building programs and extension programs. U.N. agencies did as well. Today these agencies support little research. For practical purposes, support for NARs and most extension programs is provided by the World Bank (and other banks and bilateral programs to a lesser extent). It is possible that World Bank support will be reduced in the future. The Inter-American Development Bank (IDB) is proposing a regional research fund for Latin America that effectively ends IDB support for IARCs and NARs. NARs in advanced countries will be little affected, but most weaker NARs will be substantially affected. Many have reduced their nonpersonnel budgets (in the interest of saving jobs) under budget reductions in recent years. This had debilitating effects on the effectiveness of research. D. Ten-Year Biotechnology Delay (Developing Countries). The contributions of biotechnology have been built into the nonprice terms according to the timing indicated in the scientist survey. For rice, these contributions begin early next century and become quite significant by 2015. For other crops, the timing is delayed. The biotechnology delay scenario delays the biotechnology contribution by 10 years for developing countries. We are presuming that the antibiotechnology movement will have little or no effect on developed countries, but it could easily delay access to biotechnology in most developing countries. The absence of strong intellectual property rights will also delay access to the “genes for sale” already being made available in developed countries. This scenario is supported by some nongovernmental organizations. ** E. Climate Change. A number of projections of climate change have been made in recent years. Agreement on the timing and extent of this change has not been reached. The estimates used here are that mean temperatures will rise by 1°Celsius by the year 2020 and that rainfall will increase by 3.5%. Three recent studies have provided estimates of the effects of climate change on agricultural production. The first, by Mendelsohn, Nordhaus, and Shaw (11), pioneered the use of the “Ricardian” method for relating climate change to productivity through land values. This study for the United States showed that agricultural productivity in the northern counties in the U.S. would generally increase as a result of climate change, while the warmer southern counties would experience losses. A second study for Brazil (9) found similar effects in Brazil. Municipios in the south experienced gains and those in the warmer north and central regions experienced losses. A third study for India (10) found similar effects. The three studies were sufficiently consistent in terms of fitting into a global “surface” that we believe that extrapolations to other countries (based primarily on latitude) are justified. These are the basis for the climate change scenarios (the reader should use caution, given the limited data on which the scenarios are based).

V. POLICY SIMULATIONS Global effects are summarized in Table 1 . The base case 2020/1990 ratios for production, area, trade, and prices are summarized by commodity. 2020/1990 price ratios are reported for the four policy scenarios plus a “worst-case” scenario. The base case production scenarios show that global crop production will increase by approximately 60% by 2020. Area planted to crops will expand by roughly 10%. [This includes multiple cropping so area in crops will expand by roughly 5% (mostly in Africa—see below).] Most production gains will come from yield gains. These yield gains are roughly similar to the post-Green Revolution period gains. Animal production will increase more than crop production and most of this increase will be caused by increased animal units. For beef, this indicates a significant increase in pasture land. World trade will increase for all commodities and this will take the form of increased exports by developed countries and increased imports by developing countries (see Table 2 ). Base case price projections indicate continued declines in world prices for all commodities. These projected declines are highest for rice and other grains. Table 1 also includes four policy scenarios for price ratios, and these can be directly compared with the base case price scenario. The first is the “Demographic Gift” scenario. This scenario has large price effects (note that the gift is temporary and would hold only for this period). Because of reduced demand (number of consumers), prices will fall further than base case prices for all commodities.

** Altieri, M. A. (1997) The CGIAR and Biotechnology: Can the Renewal Keep the Promise of a Research Agenda for the Rural Poor? Paper submitted for consideration by participants of consultation on biotechnology called by Consultation Group for International Agricultural Research (CGIAR) Chairman, April 18, 1997, Washington, DC.

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Delayed industrialization, on the other hand, will mean that prices will be higher than in the base case (by roughly 5%–6%). This is because of reduced private-sector R&D spillovers to agriculture. Reduced IARC–NARs support will have a larger impact on prices than delayed industrialization. Prices will be roughly 10%–15% higher than in the base case. Delayed biotechnology for developing countries also has significant price effects. These are similar to the reduced IARC–NARs support effects for crops but are smaller in magnitude than for livestock products. Global climate change effects are quite small (but see local effects, below). Price effects are only 1%–2% above the base case.

The “worst-case” calculation is the sum of the delayed industrialization, reduced IARC–NARs, delayed biotechnology, and climate change effects. In this worst case, prices of most crops will rise over the 1990 levels but not sufficiently to qualify as a “world food crisis.” Global effects, however, are really quite misleading for policy analysis as Table 2 , Table 3 , and Table 4 show. In Table 2 , base case growth rates for the 1993–2020 period for cereal crop area, yield, production demand, and food and feed demand are projected by country/region. Trade effects are the difference between demand and production. We first note that area expansion is projected to be low in most developing countries (negative in some). Area expansion will be high in most Sub-Saharan African countries because these countries have land on which to expand. This will have biodiversity habitat effects. Yield projections are actually higher for developing countries than for developed countries, reflecting the fact that they have more “catchup” potential. Production growth rates exceed demand growth rates for most developed countries (excluding Japan). This means that exports will grow at substantial rates. For most developing countries, demand growth exceeds production growth. Because of large area expansion rates, Sub-Saharan Africa countries will not have large import growth, however. Table 3 reports the area, yield, and trade 2020/1990 ratios relative to the base case for cereals by country/region for the climate change and biotechnology delay scenarios. Here we note that the local effects of climate change are important even though global effects were not. In particular, climate change has minor area effects for developed countries, but significantly increased cereals area in a number of South–Southeast Asian regions. Cereal yields will be higher in developed countries (by 1.63%) and lower in developing countries (by 1.38% including China, where they will rise). This means that climate change will produce more exports by developed countries and imports by developed countries. The biotechnology delay local effects are roughly similar to the climate change effects (recall that the base case effects were also important). Delayed biotechnology diffusion will lead to increased area cropped in all regions except the U.S.

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and Western Europe. This will have deleterious habitat consequences. Yields will be higher in developed countries and lower in developing countries. Developed country exporters will export more. Developing country importers (including China) will import more.

Table 3. Cereals: Area, yield, and trade simulations by region relative to the base case % change climate change scenario Area Yield Trade United States .0000 .0134 .0442 (X) Western Europe .0000 .0147 .0801 (X) Eastern Europe .0004 .0005 .0082 (X) Former USSR .0004 .0279 .3955 (X) Japan .0000 .0275 .0076 (–I) Developed .0003 .0163 .0816 Latin America .0007 −.0203 −.2217 (I) Sub-Saharan Africa −.0004 −.0558 −.1112 (I) West Asia–North Africa .0011 −.0370 −.0947 (I) India −.0002 −.0354 −.1132 (I) Pakistan .0006 −.0367 −.0807 (I) Bangladesh .0042 −.0299 −.1494 (I) Indonesia .0028 .0063 .0571 (I) Thailand .0071 −.0341 −.1374 (X) Philippines .0014 −.0337 −.1062 (I) Vietnam .0038 −.0303 −.2521 (X) China .0002 .0154 .0831 (I) .0007 −.0138 −.0816 (I) Developing

% change delayed biotechnology Area Yield Trade −.0018 .0006 .0532 (X) −.0003 .0012 −.0088 (X) .0072 .0097 .2553 (X) .0098 .0103 .5187 (X) .0014 .0011 .0070 (I) .0059 .0024 .0846 (X) .0131 −.0258 −.0939 (I) .0074 −.0206 −.0282 (I) .0180 −.0216 −.0183 (I) .0012 −.0238 −.0500 (I) .0027 −.0221 −.0202 (I) .0159 −.0193 −.0406 (I) .0097 −.0255 −.0353 (I) .0236 −.0266 −.0092 (I) .0080 −.0206 −.0164 (I) .0147 −.0191 −.0122 (X) .0023 −.0292 −.3196 (I) .0080 −.0259 −.0846 (I)

Table 4 reports effects of an important local welfare index in developing countries, the proportion of children 0–6 years of age who exhibit some degree of malnourishment (see Appendix for more details). First, note that this measure shows great variability in 1990 by region. The base case projections show that the percentage malnourished children will decline from 34% in 1990 to 25% in 2020 (from 1960 to 1990 it fell from 45% to 34%). This is a favorable projection, although it does vary by region (falling least in East Africa). Clearly, however, in 2020 serious local problems will remain, and they form the basis for “local food crises” even if a global food crisis is unlikely to occur. The policy scenarios show that reduced research support, delayed industrialization, delayed biotechnology, and climate change will delay progress in reducing malnutrition. The “global” effects are small, but local effects for some countries, e.g., Bangladesh and Nigeria, are significant.

VI. POLICY IMPLICATIONS Global effects of alternative policies are very poor guides to policy regarding investments and regulations affecting population and food supply. Local effects are more relevant. The simulations reported here do show that population policy can be very effective in increasing income and reducing

Table 4. Malnourished children simulation [percentage children (0-6) malnourished] Reduced research support Countries/regions Base case IARC NARs Biotech delay 1990 2010 2020 2020 2020 Latin America 20.40 16.91 14.05 14.47 14.09 Nigeria 35.4 30.79 29.52 30.21 29.86 North Africa 31.40 29.08 27.93 28.92 28.23 Central and West 22.70 22.44 21.10 21.62 21.42 Africa South Africa 24.80 22.43 21.24 21.83 21.56 East Africa 25.50 25.47 24.77 25.35 25.03 West Asia-North 13.40 11.56 9.70 10.05 9.68 Africa India 63.00 51.25 45.49 46.91 45.70 Pakistan 41.60 36.62 32.40 33.35 32.64 Bangladesh 65.80 59.20 52.85 58.12 53.86 Other South Asia 37.00 31.62 26.59 27.83 26.90 Indonesia 14.00 10.05 7.74 8.01 7.85 Thailand 13.00 7.32 5.23 5.33 5.26 Malaysia 17.60 12.41 9.88 10.05 10.00 Philippines 33.60 25.81 21.29 22.66 21.72 Other Southeast 40.00 35.69 32.78 35.21 32.98 Asia China 21.80 15.30 13.78 14.26 13.79 South Asia 58.50 47.68 41.37 43.03 41.60 34.30 28.01 25.40 26.33 25.83 Developing

Delayed industrialization 2020 14.3 29.89 28.48 21.37

Global warming 2020 14.05 30.90 31.09 21.23

21.54 25.08 9.88

21.21 24.81 9.67

46.22 32.91 55.55 27.22 7.90 5.35 10.06 22.24 34.15

45.49 32.38 53.14 26.80 7.78 5.25 9.91 21.43 33.11

14.24 42.22 26.00

13.78 41.40 25.50

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GLOBAL AND LOCAL IMPLICATIONS OF BIOTECHNOLOGY AND CLIMATE CHANGE FOR FUTURE FOOD SUPPLIES

Appendix Table A1. Industrialization ITI projections 95–00 Country United States D EC12 D Japan D Other Western Europe D Canada D Australia D New Zealand D Other Developed D Eastern Europe 2B Russia 2B Mexico 2B Brazil 2B Argentina 2B Other Latin America 2A Nigeria 1C Other Africa 1B Egypt 2A Other Near East 1C India 2A Pakistan 1C Indonesia 2B Thailand 2C Malaysia 2C Philippines 2A China and Taiwan 2C 2C Singapore

00–05

05–10

10–15

2C 2C 2C 2C 2C 2B 1C 1B 2B 2A 2B 1C 2C 2C 2C 2B 2C D

D D 2C 2C 2C 2B 2A 1C 2C 2B 2C 2A 2C 2C 2C 2C 2C

D D 2C 2C 2B 2A 2C 2B 2C 2B 2C D D 2C D

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2C 2C 2C 2B D 2B 2C 2C 2C 2C

poverty, provided the demographic gift is accompanied by effective food supply policy and investment and more generally by effective technology policy. Although it is probably the case that the coercion-based demographic gift in China is now yielding high dividends, it is not at all clear that coercion is justified in other countries. Certainly it is not justified in countries unprepared to support the gift with effective economic policy. In the past 40 years, an effective system of agricultural research centers has been built. This system has enabled the very favorable global effects realized over these years. Most local effects have also been positive, although given the starting points, indexes of poverty and malnutrition remain high in many countries in spite of local progress. The simulations reported here indicate that it is vital for local progress to continue. Shifts in the objectives of research systems and delays in bringing research technology to developing countries have high prices in terms of delayed progress on poverty reduction and land use. Without continued research to improve crop productivity, cropped area will expand, with biodiversity habitat implications.

APPENDIX: THE IFPRI–IMPACT MODEL BASE CASE IMPACT, developed at the IFPRI, is a partial equilibrium model covering 17 commodities and 35 countries/regions. It computes global equilibriums in real prices and is synthetic, in that it uses price elasticities and nonprice parameters from other studies. The model incorporates nonagricultural sector linkages but does not compute equilibriums for markets other than the 17 commodities. Each country/region submodel has a set of equations for supply, demand, and prices for each commodity and for intersectoral linkages with the nonagricultural sector. Crop

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production is determined by area and yield response functions. Area functions include price responses and a nonprice trend reflecting remaining land availability and technology. Yield is a function of the price of commodity and prices of inputs, and a total factor productivity change term. Livestock commodities are similarly modeled. Domestic demand is the sum of food, feed, and industrial use demand. Food demand is a function of prices (of all commodities), per capita income, and population. Country-specific population in growth rates are based on U.N. projections (1) Income growth is partially endogenous to the model and agriculture–nonagriculture links are specified. Feed and industrial use demands are derived from final demands. Prices are endogenously determined. Domestic prices are linked to global equilibrium prices via exchange rates, and producer–consumer subsidies and trade restrictions are allowed. Other policy instruments (acreage restrictions) are considered. Trade is determined by net supply– demand equilibrium conditions. Malnourished children projections for children (ages 0–6 years) are based on weight-for-age standards set by the U.S. National Center for Health Statistics. Data for 61 developing countries for 1980, 1985, and 1990 ‡ were used to link malnourished children proportions to per capita calorie consumption (determined in the model). The nonprice total factor productivity terms are based on a study of Indian productivity (2), a classification of industrial technological infrastructure (5), and a study of rates of return to agricultural research and extension (R.E.E., unpublished data). The ITI classification of Evenson and Westphal (5) included the following classes: Class 1A: Traditional ITI. Economics lack basic infrastructure. Government influence limited. Class 1B: First emergence. Some direct foreign investment. Class 1C: Partial modernization. Agricultural sector well developed. No R&D in producing firms. Class 2A: Mastery of conventional technology. Market skills well developed. R&D in firms. Class 2B: Transition to modern capacity. Reverse engineering capacity, sciences developed. Class 2C: Export competitiveness, adaptive invention, intellectual property rights developed. Class D: Developed country capabilities. Appendix Table A1 reports the ITI projections used in the base case. Evenson (R.E.E., unpublished data) reviews the rates of return studies used in constructing the base case. These rates of return are summarized in Appendix Table A2 . The relative median rate of return ratios for commodities and regions were used to scale nonprice terms to the rice base case terms. 1. United Nations (1992) World Population Prospects (U.N. , New York). 2. Evenson, R. E. , Herdt, W. & Hossain, M. (1996) Rice Research in Asia: Progress and Priorities (CAB International , Wallingford, U.K.). 3. Birkhaeuser, D. , Evenson, R. E. & Feder, G. (1991) Economic Development and Cultural Change 39(3) , 607–650 . 4. Evenson, R. E. , Pray, C. E. & Rosegrant, M. W. (1999) “Agricultural Research and Productivity Growth in India,” Research Report 109 (International Food Policy Research Institute , Washington, DC). 5. Evenson, R. E. & Westphal, L. (1994) “Technological Change and Technology Strategy” in the Handbook of Development Economics, eds. Srinivasan, T. N. & Behrman, J. (North–Holland, Amsterdam), Vol. 3 . 6. Huffman, W. & Evenson, R. E. (1993) Science for Agriculture (Iowa State University Press , Ames, IA). 7. Rosegrant, M. W. & Svendsen, M. (1993) Food Policy 18(2) , 13–32 . 8. Bloom, D. E. & Williamson, J. G. (1998) The World Bank Econ. Rev. 12, 419–456 . 9. Sanghi, A. , Alves, D. , Evenson, R. & Mendelsohn, R. (1997) Economia Aplicado 1(1) , 7–34 . 10. McKinsey, J. W. (1998) Ph.D. dissertation (Yale University , New Haven, CT). 11. Mendelsohn, R. , Nordhaus, W. D. & Shaw, D. (1994) Am. Econ. Rev. 84(4, 88) , 753–771 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

World food trends and prospects to 2025

TIM DYSON * Department of Social Policy, London School of Economics, London WC2A 2AE, United Kingdom ABSTRACT This paper reviews food (especially cereal) production trends and prospects for the world and its main regions. Despite fears to the contrary, in recent years we have seen continued progress toward better methods of feeding humanity. SubSaharan Africa is the sole major exception. Looking to the future, this paper argues that the continuation of recent cereal yield trends should be sufficient to cope with most of the demographically driven expansion of cereal de mand that will occur until the year 2025. However, because of an increasing degree of mismatch between the expansion of regional demand and the potential for supply, there will be a major expansion of world cereal (and noncereal food) trade. Other consequences for global agriculture arising from demographic growth include the need to use water much more efficiently and an even greater dependence on nitrogen fertilizers (e.g., South Asia). Farming everywhere will depend more on information-intensive agricultural management procedures. Moreover, despite continued general progress, there still will be a significant number of undernourished people in 2025. Signs of heightened harvest variability, especially in North America, are of serious concern. Thus, although future general food trends are likely to be positive, in some respects we also could be entering a more volatile world. The prospects for feeding humanity as we enter the 21st century often are portrayed in a daunting light. For example, we are told that the world’s population has been growing faster than cereal production since the early 1980s, and therefore that global per-capita cereal output is falling now. The rate of growth of world cereal yields also is said to be declining; the strong implication is that this decline is caused by increasing environmental production constraints. Victims of famine still appear on television, and it is clear that there are many hungry people in the world. In addition to these problems, between now and the year 2025, the human population is expected to rise from about 6 billion to 8 billion. So, especially in 1998, the bicentenary of Malthus’ Essay on the Principle of Population (1), the issue symbolized by the Chinese characters above, which together mean population (a person and an open mouth), seems very apt. With this as background and building on an earlier, much more detailed analysis (2), this paper gives my broad-brush assessment of world food prospects to the year 2025. Despite the statements of the previous paragraph, I am cautiously optimistic about our chances to better feed humanity in the next few decades. Nevertheless, the importance and complexity of the subject, the approximate nature of much of the data, the need to simplify, and the inevitable element of uncertainty when considering the future all should require no further emphasis. Because of their central place in the human diet, cereals will be my chief focus in what follows. Today, roughly half of the world’s cropland is devoted to growing cereals. If we combine their direct intake (e.g., as cooked rice or bread) with their indirect consumption, in the form of foods like meat and milk (about 40% of all grain is currently fed to livestock; ref. 3), then cereals account for approximately two-thirds of all human calorie intake. I consider prospects to the year 2025 mainly because world population projections have a fairly reliable record over future time horizons of about 30 years. My chief data sources are those of the United Nations Population Division (4) and the Food and Agricultural Organization (5, 6). This paper has three main parts. The first considers cereal and food trends during recent decades, at both the world and regional levels. The second uses demographic and cereal data to sketch what I believe is a plausible broad scenario for the future evolution of world cereal demand and supply. The final part concludes with some brief comments about the context in which the world’s farmers must grow more food.

CEREAL PRODUCTION TRENDS To consider the future we first must consider the past. Fig. 1 shows per-capita cereal production for the world as a whole since 1951, when the entire human population numbered only 2.5 billion. The annual figures for per- capita output are surprisingly variable and reflect volatility in the world’s harvest. Nevertheless, it is clear from the 5-year moving-average that world output generally has kept ahead of population growth, despite the addition of some 3.5 billion extra mouths. That said, there have been two periods of falling per-capita cereal production. The first happened around 1960 and mainly reflects the agricultural losses associated with Mao’s disastrous “Great Leap Forward” in China. The second period has been since the early 1980s. The moving-average peaks at 371 kg in 1984 and has fallen to around 350 kg in the mid-1990s. Since 1984 the world’s population has been growing faster than cereal production. Note the hint that volatility in the global harvest recently may have increased. The fact that world population growth has been outpacing cereal production since 1984 readily attracts attention, but interpreted without any qualification, it is seriously misleading for two reasons. First, it hides the fact that much of the recent decline in world cereal production has occurred in relatively well-fed regions. Second, it does not account for the fact that the regional composition of humanity is changing. In particular, most demographic growth is happening in parts of the world with low levels of per-capita cereal consumption and, other things being equal, this fact tends to weight downward

* To whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org. Abbreviations: FSU, former Soviet Union; EU, European Union; ha, hectare.

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the average level of world per-capita cereal consumption (and hence production).

FIG. 1. World per-capita cereal production, 1951–1997. Averages for 1952 and 1996 are calculated from data for 1951–1953 and 1995–1997, respectively. Here and subsequently cereal data are expressed in production terms. Principal data sources: refs. 4 and 5 . Adapted from ref. 2 . Regional Cereal Production Trends. A better picture emerges if regional trends are considered. The present work arranges the world’s countries into seven regions (see ref. 2 for details). Six appear in Fig. 2 . I discuss them in turn. Sub-Saharan Africa has done very poorly in terms of food production. The explanation has many sides, but it includes ethnically heterogeneous nation states, widespread political instability, neglect of agriculture by governments, and, despite its many health problems (including the AIDS epidemic), extremely rapid population growth. The distinctiveness of crops and farming methods in this region also has meant that it has often missed out on “Green Revolution” technical developments (e.g., relating to high-yielding varieties of wheat and rice) that have boosted agricultural production elsewhere. Around 1995 this region’s average per-capita cereal output was only about 146 kg, which is a low figure, even allowing for the fact that cereals are not grown in much of middle and west Africa, and average levels of per-capita cereal consumption were only slightly higher because of cereal imports and aid. Fig. 2 shows a generally declining trend in per-capita output from the 1960s onward. There are also signs of heightened harvest variability. The droughts of 1983, 1984 (when there was major famine in Ethiopia), and 1992 are very clear. The Middle East here combines North Africa and West Asia. Fig. 2 shows that this region has experienced a significant long-run decline in its per-capita output, which is not helped by its rapid demographic growth. The annual volatility of the harvest in this water-scarce area is also striking. Average levels of per-capita cereal production during the 1990s have fluctuated between 250 and 270 kg, with no particular trend apparent since the early 1980s. However, the Middle East imports large quantities of cereals, mostly from North America. Around 1990 these imports accounted for almost a third of the region’s entire cereal consumption, and they raised the average level of per-capita consumption to about 386 kg. These imports (which

FIG. 2. Per-capita cereal production by world region, 1951–1997. Averages for 1952 and 1996 are calculated from data for 1951–1953 and 1995–1997, respectively. Principal data sources: refs. 4 and 5 .

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often are used to feed livestock) can be seen as an oblique way of importing water. South Asia mainly comprises the populous countries of the Indian subcontinent (India, Pakistan, and Bangladesh). The trend in Fig. 2 is dominated by India, which contains around 70% of the region’s people. The 5-year curve shows the effects of significant famines in the mid-1960s and early 1970s, which cost lives. But during the last two decades there has been no major food crisis, and average levels of percapita cereal output have risen to around 225 kg in the mid-1990s. Notice that despite the plateau of the 1990s, levels of per-capita production are still significantly higher than those of the early 1980s. Note, too, the hint of a remarkable recent reduction in harvest variability. East and Southeast Asia is dominated by China, although it includes other major populations, especially Indonesia and Japan. This region’s trend in Fig. 2 clearly reflects the agricultural output losses of China’s calamitous “leap” around 1959–1964, when perhaps 20 million-30 million died in famine. However, the subsequent trend in per-capita cereal production generally has been upward. Notice the sharp acceleration after the agricultural policy reforms that were introduced in China around 1978. This acceleration also reflected the introduction of hybrid rice and, still more, large increases in the use of chemical fertilizers by Chinese farmers. This region has continued to experience a rise in average per-capita cereal output since the early 1980s, albeit at a slower rate. By the mid-1990s regional production averaged about 316 kg per head. It is obvious that the last two regions in Fig. 2 hold the key to the decline in world per-capita output since 1984. The first is Europe, here including the countries of the former Soviet Union (FSU). The second is North America/Oceania, a hybrid region, essentially comprising the traditional major cereal exporters of Canada, Australia, and, above all, the United States. Both of these regions produce cereals in comparative abundance. In the mid-1990s the average per-capita output in Europe/FSU was about 530 kg, and the figure for North America/Oceania exceeded 1.2 tons per person. Although the U.S., Canada, and Australia together contain less than 6% of the world’s population, they currently produce about 20% of the global cereal harvest. To understand why Europe/FSU and North America/ Oceania both have experienced recent declines in per-capita cereal production requires a little history. In brief, the story is as follows. In the decades after the Second World War, until the 1970s, the countries of Western Europe, particularly those that now form the European Union (EU), were major net cereal importers from the three traditional exporters of North America/Oceania. In the 1980s this situation changed, because the EU, with its heavily protectionist Common Agricultural Policy, rapidly emerged on the world stage as a significant rival cereal-exporting bloc, which offloaded cereal surpluses on the international market at heavily subsidized prices. In turn, this provoked retaliatory responses from the traditional cereal exporters, especially the U.S., and by 1990 world grain prices were exceptionally low, at roughly 60% of their 1980 level. Neither of the key players in this drama (the U.S. and EU) could avoid the fundamental logic of the situation. Accordingly, both have had to introduce policies designed to reduce cereal support costs, decrease stocks (which are expensive to maintain), and reduce their cereal cropland through the idling of significant areas of land. That said, the policy response has been much swifter in the United States (and Canada and Australia) than in Europe. Because many European countries benefit from the Common Agricultural Policy the policy has been hard and slow to change. Indeed, the chief cause of the really precipitate recent decline in per-capita cereal output shown in Fig. 2 for Europe/FSU lies elsewhere. The main explanation for the cereal output collapse of the 1990s has been the massive economic and political disruption resulting from the fall of communism in eastern Europe and the FSU. Consider, for example, that in 1990 the Soviet Union had a near-record cereal harvest of 227 million tons, but by 1995 the component countries of the FSU produced only 122 million tons of cereals. A decline of 105 million tons is roughly equivalent to losing production equal to about 4 years of growth in world cereal demand. Finally, a word is in order regarding Latin America, the region not shown in Fig. 2 . Levels of per-capita cereal output in Latin America are relatively low, around 260 kg in the mid-1990s (although cereals are probably a poorer proxy for food in general here than is the case for any other developing region). The trend for Latin America is actually very similar to that shown for North America/Oceania in Fig. 2 . In particular, per-capita cereal output declined from a peak in the early 1980s to a trough around 1990, and then there was a period of limited recovery in the 1990s. The explanation for this similarity of trend is the common influence of international market conditions, notably as they affected Argentina, which is the region’s second biggest cereal producer (after Brazil) and the largest exporter by far. Confronted by a steadily deteriorating world price, Argentina’s farmers had little choice but to shift large areas of land out of wheat in the 1980s. Concluding Remarks on Recent Trends. I conclude this review of past trends with six comments. First, it should be clear that world cereal production has grown more slowly than population growth chiefly because of deliberate policies and political developments in North America/Oceania and Europe/FSU. With the exception of Latin America (a special case) average percapita cereal output in the mid-1990s exceeded that in 1984 in all other world regions. It is especially noteworthy that the two large Asian regions, which together contain 57% of humanity, both have experienced significant rises in per-capita cereal production. Second, those who point to a “dramatic slowdown” in world cereal yields (see ref. 7, p. 142) are mistaken. Fig. 3 shows that the trend is more or less linear, or “arithmetical” to use Malthus’ term. Of course, on a rising base this linear trend translates into a declining percentage increase, but that is inevitable. There was a brief yield pause in the early 1990s, largely because of major yield declines in the former communist states of Europe/FSU. But in the last few years the global yield has resumed its upward march. My earlier research (2) took the world yield around 1990 of 2.711 metric tons per hectare (ha) and projected it forward by using the average slope of +42.6 kg/ha per year experienced during 1981–1993. This procedure implies a 1997 yield of 3.009 tons/ha, only very slightly higher than the actual yield of 2.979 tons (see ref. 6). Inasmuch as anything can be gleaned about regional yield trends in the brief period since 1993, then sub-Saharan Africa and the Middle East have done poorly. But both South Asia and East and Southeast Asia have performed much as projected on the basis of their yield trends during 1981–1993, and

FIG. 3. World cereal yield, 1951–1997. Principal data source: ref. 5.

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Latin America and North America/Oceania have done better still. It is important to appreciate that it is inevitable that there is annual fluctuation in the world yield. And periods of plateau, particularly in certain locations and for specific crops, are an integral feature of overall yield advance. Thus, with generally low international prices, the 1990s have seen indifferent yield performance for wheat. We cannot be complacent, but there is no particular cause for concern about recent world cereal yield trends. Third, the basic relationships linking volumes of world cereal stocks, world cereal aid donations, and international cereal prices during recent decades are fairly clear. Fig. 4 shows that stock and donation levels have tended to vary directly with each other and inversely with prices. After my preceding discussion of the recent rivalry between the U.S. and EU, notice how the level of world cereal stocks has fallen sharply since the peak of the 1980s, largely because of their shared policy need to run down the size of their publicly held stocks. This common policy objective may partly explain why in the early 1990s cereal aid donations were somewhat higher than might have been anticipated given previous experience. However, a more important part of the explanation was the sudden appearance of new recipients for aid, i.e., the collapsed former communist states. Fourth, of course, we do not live by cereals alone. There is considerable evidence that in most world regions human diets have become more diverse since the early 1980s (e.g., see refs. 8 and 11). As living standards generally have risen and populations have urbanized, so consumption and production levels of fruit, vegetables, livestock products, and processed foods all have tended to rise, too. In this context the Food and Agricultural Organization calculates indices of per-capita food output, which use price data to weigh estimates of the production quantities of all the main types of food. For the developing world as a whole this index was 114 in 1990–1992 (1979–1981 = 100; see ref. 12); only for sub-Saharan Africa do these indices suggest that food output has not been able to keep up with population growth. Increases in noncereal food output have been especially marked in South Asia (a corresponding index of 117) and, still more, East and Southeast Asia (index of 128), reflecting significant gains in India and China, respectively. So the evidence is strong that in most parts of the world human diets have been becoming more varied. And in many locations cropland that has been shifted out of cereals, because of their low relative prices, has been switched to grow other food and nonfood crops. Fifth, both the frequency and demographic impact of famines have been considerably reduced, which is part of the message from Fig. 2 . However terrible they may be, recent events in places like North Korea and southern Sudan are probably less than those that engulfed countries like Mozambique and, certainly, Ethiopia in the 1980s. And they are certainly small compared with the major famines of the early 1940s, or the Chinese calamity around 1960. From all of these cases it is obvious that warfare and dislocation arising from political upheaval are the chief causes of famine in the modern world. The role of agricultural production failure, by itself, is comparatively small. Moreover, nowadays ways to combat what is usually the principal proximate cause of famine deaths (epidemic disease) generally are improved, although they cannot always be implemented. Today famine has become largely a sub-Saharan tragedy, and even there one authority has described the chances of an African dying in a famine as “vanishingly small” (see ref. 13, p. 31).

FIG. 4. World cereals: prices, stocks, and donations, 1960–1997. Principal data sources: refs. 3 and 8 , 9 – 10 . Adapted from ref. 2 . Finally, for two reasons, we now may be entering an era of rather greater international cereal price volatility than has prevailed for some time. One reason is the lower level of world cereal stocks, itself conditioned by the recent policies of the U.S. and EU. Undoubtedly, this lower stock level influenced the sudden cereal price rise of 1996, although it is worth noting that even in 1996 the international price was probably no higher than in 1985 or 1989 (see Fig. 4). It may be that any “trigger point” of world cereal stocks, below which some writers (14) suggest grain prices will become more variable, has shifted downward. The second reason is the worrying rise of cereal harvest volatility in North America. It should be stressed that for five of the seven regions in this study there are no signs of any increase in cereal harvest variability (see ref. 2). Indeed, for South Asia I already have remarked on a seeming recent diminution of harvest fluctuations, which are related to a series of good monsoons, which may be a beneficial result of climate change. Sub-Saharan Africa has experienced a long-run rise in harvest volatility, but this rise has a negligible impact on world output because the region produces less than 5% of the global harvest. However, just a glance at Fig. 2 reveals the major rise in North America’s harvest volatility. This rise is important because the region is still the main supplier of cereals to world markets. This increased volatility in North America is largely weather-induced (witness the output declines of 1983, 1988, 1993, and 1995), and it is possibly a negative result of climate change.

THE FUTURE: CEREAL DEMAND AND SUPPLY So, although not without problems, recent trends have not been as dismal as they sometimes are portrayed. And, in turn, this conclusion allows me to make some speculations about the future that are more upbeat than downbeat, though with elements of both beats. Inevitably, what follows is very broad-brush, and it involves a mixture of projection, extrapolation, and judgment (for more detail and qualification see ref. 2). I first will examine the evolution of world cereal demand, and then consider supply. Although there are different approaches to estimation (see ref. 15) there is little doubt (i) that since the 1950s population growth has been responsible for a rising share of world cereal demand growth, and (ii) that population growth will be the chief cause of cereal demand growth in the period to 2025. Table 1 gives some illustrative calculations based on the United Nations’ 1996 “medium variant” (essentially best-guess) population projections to the year 2025. And following my earlier work, I use 1990 as the base year. Table 1 shows that in the period to 2025 the world’s population is expected to rise by just under 800 million per decade, to slightly over 8 billion. The largest absolute additions, by far, will occur in South Asia and sub-Saharan Africa. These are regions of low per-capita cereal production and consumption, but together they account for more than 55% of the total anticipated demographic growth. An initial calcula-

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Table 1. Regional projections of population and cereal demand (millions of tons) 1990–2025 Population, millions Cereal consumption in 1990 Projected cereal demand in 2025 based on Region 1990 2025 Per capita, kg Volume, mill. tons Population increase Population plus only income Sub-Saharan Africa 490 1,197 150 73.6 179.8 179.8 The Middle East 276 534 386 106.6 206.4 231.9 South Asia 1,193 2,021 237 282.2 478.1 549.7 East and Southeast 1,794 2,387 338 605.8 806.2 1,040.9 Asia Latin America 440 690 265 116.6 182.7 217.9 Europe/FSU 788 799 634 499.3 506.5 506.5 North America/ 304 410 780 237.1 319.5 319.5 Oceania 5,285 8,039 363 1,921.3 2,679.0 3,046.5 World Following previous work (2), I retain 1990 as the base year for projection. The estimated demand on population plus income assumes no change in per-capita cereal consumption in sub-Saharan Africa, Europe/FSU, and North America/Oceania. However, in the remaining regions rises are assumed, taking average per-capita cereal consumption in 2025 to 434 kg (in the Middle East), 272 kg (South Asia), 436 kg (East and Southeast Asia), and 316 kg (Latin America). For details of the basis of these assumptions see ref. 2 . Principal sources: refs. 2 , 4 , and 5. tion of the volume of world cereal demand in 2025 holds per-capita cereal consumption constant in each region (at the levels prevailing around 1990) and then projects demand forward solely on the basis of the anticipated population growth. Table 1 shows that on this populationincrease-only assumption, world cereal production must rise from around 1.921 billion tons in 1990 to about 2.679 billion in 2025 to match the rise in demand. Note, too that, on this basis, world per-capita cereal production would fall to 333 kg (2,679/8,039) simply because of the changing regional composition of humankind (i.e., even though per-capita consumption levels would stay constant in each region). This fall illustrates my previous point that very different regional rates of demographic growth have implications for global cereal demand that, to the extent that demand stimulates supply, are weighing downward average levels of world output. Of course, levels of per-capita cereal consumption will not remain constant. Rising incomes will increase levels of consumption in some regions; although, in others, health concerns about eating meat could reduce levels of per-capita intake. Also, factors like population aging and urbanization could exert a modest influence on the evolution of future world demand. Although no one can predict how these factors will evolve, a second set of calculations can capture some of the broad implications. Accordingly, I believe it plausible to assume some continued rise in overall per-capita cereal consumption in the Middle East, South Asia, Latin America, and, most importantly, East and Southeast Asia. Essentially, this computation has been done by means of a considered extrapolation from the corresponding regional per-capita cereal consumption trends of the period 1970–1990 (see ref. 2). The resulting average levels of per-capita cereal consumption in 2025 assumed here for the four regions are given in the notes to Table 1 . However, the poor record of sub-Saharan Africa means that I have retained the assumption of constant per-capita consumption for this region. And the same applies for both Europe/FSU and North America/Oceania, although here my rationale is that levels of per-capita consumption are unlikely to rise from those prevailing around 1990, and they could even decline (for example with a reduction in demand for livestock products). The conjectural nature of these calculations should require no emphasis. However, the population plus income column of Table 1 suggests that roughly 3 billion tons of cereals will have to be produced in 2025 to match the volume of world cereal demand. Can the world’s farmers produce 3 billion tons for 8 billion people in 2025? Preliminarily, the evidence already reviewed suggests that they probably can, or, at least, something very close to it. Although the trend in world per-capita cereal output is rather misleading (partly because the regional composition of humanity is changing) the trend in the world cereal yield (see Fig. 3) is more telling, because the regional composition of the world’s harvested cereal area has changed less. And, clearly, it is yields that hold the answer to future world food production. If from 1990 we extrapolate the world cereal yield in Fig. 3 on the previously mentioned average increment for 1981–1993 (of 42.6 kg/ha per year) then the average yield in 2025 will be around 4.20 tons. And coupled with the world harvested cereal area around 1996 (of about 702 million ha) this yield alone would produce 2.95 billion tons of grain. Even by using the average increment experienced since 1990 (of about 38.3 kg/ha) gives a yield of 4.05 tons in 2025 with corresponding output of 2.85 billion tons. Moreover, these calculations do not allow for any increase in harvested cereal area. Furthermore, here I have projected demand and supply independently, but, of course, in the real world they continually interact. The scope for adjustment between the evolution of global cereal demand and supply, e.g., in terms of changes in consumption patterns, or areas of cropland sown with cereals, is considerable. However, again, matters are better considered at the regional level. Accordingly, Table 2 summarizes some simple calculations regarding regional yields. I stress that they are not meant as detailed projections, but rather as a backcloth for discussion. Again 1990 is taken as the base year. The first two columns provide the regional cereal areas harvested and corresponding yields around 1990. The third column gives the average annual increments in yield experienced over the period 1981–1997, broadly the period for which some authors (7) claim to detect major problems in world cereal yield growth. The fourth column shows what the regional cereal yields will be in 2025 on the assumption that the average increments experienced for 1981–1997 continue into the future. The fifth column gives the corresponding levels of cereal production in 2025 on the assumption that the areas harvested remain constant as around 1990. And the final column shows the regional shortfalls or surpluses implied when these production figures are compared with the previous projections of demand. The broad picture that emerges from Table 2 , to which I fully subscribe, is that there is going to be an increasing degree of regional mismatch between the expansion of demand and the capacity to meet that demand. In general, the world’s developing regions are going to increasingly depend on cereal imports, both in absolute terms and as a proportion of their total consumption. So the volume of world trade in cereals must rise, probably more than doubling between 1990 and 2025. The U.S., Canada, and Australia will continue as the main source of cereals for world markets, but increasingly they will be joined in a subsidiary role by Europe/FSU. Notice that even on these rough illustrative assumptions the total global

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shortfall is only 68 million tons; although, to reiterate, there is considerable scope for adjustment. I now look briefly at the prospects for each region.

Table 2. Projected cereal yields and production in 2025 by region Average area Average Average Region harvested yield, 1989– annual cereal 1989–1991, 1991 yield million ha increase, kg/ ha per year 1981–1997 Sub-Saharan 59.3 1.165 10.6 Africa The Middle 40.2 1.642 23.6 East South Asia 140.3 1.919 52.0 East and 145.1 3.817 70.9 Southeast Asia Latin America 48.4 2.119 40.5 Europe/FSU 171.4 2.816 22.8 North America/ 98.4 3.734 55.4 Oceania 703.1 2.711 39.0 World

Linearly projected yield 2025

Projected production on the basis of constant area, million tons

Shortfall/ surplus compared to projected demand

1.536

91.1

−88.7

2.468

99.2

−132.7

3.739 6.299

524.6 914.0

−25.1 −126.9

3.537 3.614 5.673

171.2 619.4 558.2

−46.7 +112.9 +238.7

4.076

2,977.7

−68.5

The total 2 025 cereal production figure given above is the sum of the regional figures, as is the total shortfall. I stress that the above figures are simply a backcloth for discussion. They are based on the unlikely assumption of no change in harvested cereal area. A quantitative integration of broadly plausible area changes is available elsewhere (see ref. 2 ). Principal sources: refs. 2 , 4 , and 5 . Sub-Saharan Africa is unlikely to see much improvement in its overall food situation. The population is expected to more than double between 1997 and 2025, but there is nothing in the region’s agricultural history to suggest that it will increase its food output to meet the demographically driven expansion of demand. Average yields may not rise much, and despite the assumption of Table 2 increases in food output often will come from an expansion of the cropland area. It seems highly unlikely that the annual volume of cereal imports (including cereal aid) will increase to anywhere near 88 million tons by 2025. Only a minority of countries will be able to afford to buy sizable amounts of food, and this fact alone may reduce much of any 68 million ton global shortfall such as is implied by Table 2 . It is conceivable that per-capita food consumption in the region could decline. Surely, and above all, sub-Saharan Africa deserves attention and assistance, both apropos agriculture (on the supply side) and reproductive health/family planning (on the demand side). Moreover, despite all of its problems, it is important to acknowledge the region’s tremendous potential. Furthermore, there are some encouraging recent developments, like falling birth rates now in most countries, and signs (admittedly very weak) of a democratic wave, notably, but not only, in South Africa (16). In the long run progressive political change may be vital for helping to solve this region’s many problems. The Middle East certainly will depend even more on cereal imports in the next few decades. Indeed, it is perfectly possible that this region could be meeting half (or more) of its total cereal consumption through imports by 2025. Water constraints and population growth are parts of the explanation for this situation. Most countries in the region are likely to be able to finance most of their imports. For example, some have oil reserves or benefit from tourism. Other countries, such as Egypt, will finance their imports partly through the export of specialist foods to Europe, where they already provide rising competition for growers in locations like Spain and Greece. However, Sudan is one major country that will almost certainly have difficulty in purchasing sufficient cereal supplies. And Sudan is a vivid reminder of the region’s general political instability, which could profoundly affect national levels of food security in the coming decades (for a quantitative attempt to integrate sociopolitical stability into estimates of national food security see ref. 2). South Asia emerges from Table 2 with the smallest projected regional cereal shortfall, whether measured in absolute or proportional terms. There are several reasons for thinking that this region will not develop a huge cereal import requirement despite its considerable future population growth. First, there is South Asia’s current low level of per-capita cereal consumption, which remains comparatively low even if a significant increase during the period to 2025 is incorporated. Of course, this outlook is not a happy consideration, because it reflects widespread undernourishment, but it is a fact. Second, there is the commonly prevailing vegetarian diet. This diet may diminish, especially in urban areas, thereby raising the indirect consumption of grain. However, vegetarianism certainly will stay as a strong influence in the next few decades, and it will restrain the growth of total cereal demand. A final reason cereal imports may rise only modestly in the coming decades is that the current average regional yield is low, suggesting scope for improvement. Note in Table 2 that even the linearly projected cereal yield for 2025 is below that which prevailed in East and Southeast Asia around 1990. Much of the recent, and future, rise in South Asia’s yields will come from greater use of chemical fertilizers. For example, in India the level of annual applications has risen from 49 to 80 kg/ha of cropland between 1984 and 1994, and a similar story applies for both Pakistan and Bangladesh (see ref. 3). Table 1 suggests that East and Southeast Asia is the only region where, especially given the presence of China, future economic growth could have a broadly comparable impact on the growth of total cereal demand as will future population growth (of course, this region’s demographic growth is rapidly slowing). So, irrespective of the numbers in Table 2 , it seems very probable that East and Southeast Asia will have the largest absolute cereal import requirement of any region in 2025. That said, there seems to be no particular reason for alarm regarding the growth of China’s cereal demand. The country has important agricultural potentials (e.g., the upgrading of grasslands); until recently its cropland area probably has been seriously underestimated and, relatedly, its yields overestimated (see e.g., refs. 17 and 18). China’s recent performance in raising cereal yields has been, and continues to be, strong. Finally, the country’s political leadership is very aware of the importance of increasing national food output as demand rises (recall the characters at the beginning of this paper). So when some people (19) ask “who will feed China?” The answer is plain: mainly, the Chinese. China and East and Southeast Asia as a whole will significantly increase their volumes of cereal imports but almost certainly not to the massive levels that some (7, 19) have suggested. Again, as everywhere, sociopolitical stability will be a crucial ingredient for continuing food security. And if this component is factored in, then by some reckoning China may be no more food secure than India, despite its better agricultural performance (2). Latin America has relatively favorable prospects. Of course, some countries (e.g., Peru and Bolivia) have major food

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problems. And in most countries there are significant food difficulties arising from inadequate purchasing power among poorer sections of the population (although overnutrition is an increasing problem in much of the region, too). However, the region as a whole is comparatively advanced, demographically, economically, and politically. As previously intimated, focusing on cereals can be misleading because Latin America is a major producer and exporter of products like sugar, soybean, meat, coffee, cocoa, and vegetables. Should cereals become more profitable in the decades ahead then Argentina and perhaps Brazil could become significant cereal exporters, for example, to China. Finally, this brings me to the two main exporting regions, Europe/FSU and North America/Oceania. Table 2 implies annual net cereal exports from Europe/FSU exceeding 110 million tons by around 2025, which seems plausible. Note that this surplus results from extrapolating the very modest annual yield increment of only 22 kg/ha per year experienced during 1981–1997. The small size of this increment was almost entirely the outcome of the yield collapse experienced in Eastern Europe and the FSU. In fact, an average increment closer to 47 kg for this region is perfectly credible over the longer run (see ref. 2). There will be continued major yield rises in the EU. Here are two recent illustrations: between 1989–1991 and 1995–1997 France’s average cereal yield rose from 6.24 to 6.81 tons, and the United Kingdom’s, from 6.17 to 6.98 tons. Consequently, the amount of idled cereal land in the EU may well be raised, although it also could be reduced (i.e., more land could be brought into cultivation if the need arose). In addition, there is great potential to raise cereal production in Eastern Europe (notably Poland) and large areas of western Russia, Ukraine, and Kazakhstan in the FSU. Undoubtedly, reforming the farming sector in most of these former communist countries is proving to be a lengthy and extremely difficult process. It is complicated by issues of access to European markets and applications for EU membership. In turn, these issues raise the important problem of Common Agricultural Policy reform. Finally, the capacity for continued cereal yield and output growth in North America/Oceania is also strong. Again, comparing averages for 1989–1991 and 1995–1997, and in increasing order of export importance, cereal yields rose from 1.66 to 1.91 tons/ha in Australia, 2.47 to 2.69 tons in Canada, and 4.58 to 5.04 tons in the U.S.. With an average yield for the region of 4.08 tons in 1995–1997, an average of around 5.5 tons in 2025 seems to be a realistic target. Indeed, the average regional yield in 1994 was nearly 4.5 tons [assisted by good U.S. out-turn for maize (corn)]. To reiterate, a greater problem apropos production in this region may be increasing harvest volatility, with obvious implications for world prices. The other regional prospect of which we can be sure is that there will be continued agricultural rivalry with the EU, which will extend far beyond cereals.

CONCLUSION Inevitably this paper has omitted a lot, and one’s view as to whether the prospects to 2025 are good or bad depends partly on the particular criteria that are used. Surely the prospects are mixed. However, in my view, over this specific time horizon, they are more good than bad. In 2025 the world’s farmers will be producing roughly 3 billion tons of cereals to feed the human population of around 8 billion, which will require an average world cereal yield of about 4 metric tons/ha (see also ref. 20). It also is likely that some regions will, for different proximate reasons, experience an increase in their harvested cereal area. For example, in sub-Saharan Africa with meager yields this increase may happen because of population growth, whereas in Latin America it could happen to meet export demand. We know that there are significant problems of soil structure when land is cultivated year after year (e.g., see ref. 24). But problems of water for agriculture probably will be much more important. World agriculture will have to use its water supply very much more efficiently in the coming decades. And water is a resource that must be better priced. Of course, there will be new crops and improved seeds. But most of the required increase in the world’s harvest will come from the application of procedures and knowledge that we already have to the current world harvested area. It is inescapable that humanity will depend even more on synthetic nitrogen fertilizers for its food supply (e.g., see ref. 21). My calculations using Gilland’s equations (22) suggest that there may have to be an approximate doubling of global use of synthetic nitrogen to produce 3 billion tons of grain (2). Another vital resource for the future will be a continuing rise in the level of population, and hence farmer, education in most regions. And farming everywhere is likely to involve much greater dependence on information-intensive farm management procedures, as well as heightened attention to variation of conditions within individual fields, whether done through the reading of subtle color change in crop leaves or by satellite imagery. It is highly unlikely that there will be any wonder breakthrough that will solve the problem of raising world food production. On the contrary, it will continue to be hard work. Moreover, the process of raising yields and agricultural advance is extremely complex. Many of the multitude of developments that together will influence the world food outlook (e.g., relating to education, health conditions, technology, transport and communications, and institutional structures) primarily are fashioned by the wider world, i.e., beyond agriculture itself. Crucial among these will be developments in the realm of political economy. Almost everywhere socio-political stability will be the most important element for maintaining food security in the future. I have noted the importance that political reform could have in sub-Saharan Africa over the longer run. Then there is the issue of how the situation in Eastern Europe and the FSU (and reform of the Common Agricultural Policy) will unfold. There is also the related matter of international trade arrangements, where it seems probable that the momentum toward increasing liberalization will be maintained. Partly for this reason, it is hard to envisage that average world food prices will be higher in 2025 than applied, say, in the early 1990s (see ref. 23), although prices could well be more volatile. There will still be many hungry people alive in the year 2025. But if the scenario envisaged by this paper applies, then there must be a reasonable chance that the absolute number will be fewer than is the case today. Also, we should not lose sight of the rapidly growing problem of overnutrition in some urban areas of the developing world. However, the very substantial demographic growth that will happen in the world’s worst-fed regions almost guarantees the continuation of a considerable volume of undernourishment. Significant areas, especially in sub-Saharan Africa, may effectively remain “lost” to development, including agricultural development. In such locations population growth will contribute to environmental damage as people try to eke out a bare living from the land. In conclusion, the main thrust of this paper has been to show that, in general, the world food situation has been improving. And I have argued that this trend probably will continue during the next few decades. World food output will continue to rise, although there will be a growing degree of mismatch between the expansion of food demand and the capacity to supply that demand. Accordingly the balance will be met by a considerable expansion of the world food trade. As a result, most people probably will be better fed in 2025 than is the case today.

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This work was funded partly by the United Kingdom Economic and Social Research Council (Economic and Social Research Council Award L320-27-3024). 1. Malthus, T. R. (1798) An Essay on the Principle of Population (Johnson , London). 2. Dyson, T. (1996) Population and Food: Global Trends and Future Prospects (Routledge , London). 3. The World Resources Institute , United Nations Environment Program , United Nations Development Program & World Bank (1998) World Resources 1998–99 (Oxford Univ. Press , New York). 4. United Nations (1996) World Population Prospects: The 1996 Revision (United Nations , New York). 5. Food and Agricultural Organization (1951–1997) Production Yearbook (Food and Agricultural Organization , Rome). 6. Food and Agricultural Organization (1998) FAO Quarterly Bulletin of Statistics (Food and Agricultural Organization , Rome). 7. Brown, L. R. & Kane, H. (1995) Full House (Earthscan , London). 8. Mitchell, D. O. & Ingco, M. D. (1993) The World Food Outlook (The World Bank , Washington, DC). 9. Brown, L. R. (1998) in Vital Signs, 1998, 1999, eds. Brown, L. R. , Renner, M. , Flavin, C. & Starke, L. (Earthscan , London), pp. 38–39 . 10. Food and Agricultural Organization (1983–1997) Food Aid in Figures (Food and Agricultural Organization , Rome). 11. Mitchell, D. O. , Ingco, M. D. & Duncan, R. C. (1997) The World Food Outlook (Cambridge Univ. Press , Cambridge). 12. Dyson, T. (1994) Popul. Dev. Rev. 20, 397–411 . 13. Seaman, J. (1993) Inst. Dev. Studies Bull. 24, 27–31 . 14. Brown, L. R. (1998) in State of the World 1998, eds. Brown, L. R. , Flavin, C. & French, H. F. (Earthscan , London), pp. 79–95 . 15. Alexandratos, N. (1997) Popul. Dev. Rev. 23, 877–888 . 16. Lansner, T. R. (1995) in Freedom in the World, eds. Adrian Karatnycky, I. R. , Cavanaugh, K. , Finn, J. , Graybow, C. , Payne, D. W. , Ryan, J. E. , Sussman, L. R. & Zarycky, G. (Freedom House , New York), pp. 25–30 . 17. Alexandratos, N. (1996) Agric. Econ. 15, 1–16 . 18. Crosson, P. , ed. (1996) Perspectives on the Long-term Global Food Situation 2 (Federation of American Scientists Fund , Washington, DC), pp. 1–8 . 19. Brown, L. (1995) Who Will Feed China: Wake-up Call for a Small Planet (Norton , New York). 20. Evans, L. T. (1998) in Feeding a World Population of More than Eight Billion People, eds. Waterlow, J. C. , Armstrong, D. G. , Fowden, L. & Riley, R. (Oxford Univ. Press , New York), pp. 89–97 . 21. Smil, V. (1997) Sci. Am. 277, 58–63 . 22. Gilland, B. (1993) Endeavour New Ser. 17, 84–88 . 23. Winkelmann, D. L. (1998) in Feeding a World Population of More than Eight Billion People, eds. Waterlow, J. C. , Armstrong, D. G. , Fowden, L. & Riley, R. (Oxford Univ. Press , New York), pp. 264–272 . 24. Cassman, K. (1999) Proc. Natl. Acad. Sci. USA 96, 5952–5959 .

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PLANT GENETIC RESOURCES: WHAT CAN THEY CONTRIBUTE TOWARD INCREASED CROP PRODUCTIVITY?

5937

This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Plant genetic resources: What can they contribute toward increased crop productivity?

DAVID HOISINGTON * , MIREILLE KHAIRALLAH , TIMOTHY REEVES , JEAN MARCEL RIBAUT , BENT SKOVMAND , SUKETOSHI TABA , AND MARILYN WARBURTON International Maize and Wheat Improvement Center (CIMMYT), Lisboa 27, Apartado. Postal 6-641, 06600 Mexico City, Mexico ABSTRACT To feed a world population growing by up to 160 people per minute, with >90% of them in developing countries, will require an astonishing increase in food production. Forecasts call for wheat to become the most important cereal in the world, with maize close behind; together, these crops will account for
80% of developing countries’ cereal import requirements. Access to a range of genetic diversity is critical to the success of breeding programs. The global effort to assemble, document, and utilize these resources is enormous, and the genetic diversity in the collections is critical to the world’s fight against hunger. The introgression of genes that reduced plant height and increased disease and viral resistance in wheat provided the foundation for the “Green Revolution” and demonstrated the tremendous impact that genetic resources can have on production. Wheat hybrids and synthetics may provide the yield increases needed in the future. A wild relative of maize, Tripsacum, represents an untapped genetic resource for abiotic and biotic stress resistance and for apomixis, a trait that could provide developing world farmers access to hybrid technology. Ownership of genetic resources and genes must be resolved to ensure global access to these critical resources. The application of molecular and genetic engineering technologies enhances the use of genetic resources. The effective and complementary use of all of our technological tools and resources will be required for meeting the challenge posed by the world’s expanding demand for food. Today, on the eve of a new millennium, we are approaching a critical era in the evolution of our planet and species—we are in a race between growing population and food production. This era was cast in Paul Ehrlich’s The Population Bomb (1), perhaps prematurely, as a time when population would outpace the earth’s resources, including its capacity to produce food. The threat of the Malthusian crisis forecast by Ehrlich appears to have diminished as we have witnessed a slowdown in the rate of population growth. But the challenge of feeding a world population growing by up to 160 people every minute (>90% of them in developing countries) remains daunting. It is forecast that, by 2050, world population will increase from the current level of
6 billion to >8 billion people. Feeding this population will require an astonishing increase in food production. In fact, it has been estimated that the world will need to produce as much food during the next 50 years as was produced since the beginning of agriculture 10,000 years ago (2)! Today, it appears more likely that a population/food crisis may be born, not from an exponentially increasing world population (though in some of the world’s poorest regions, population growth remains exceedingly high), but from an ill-founded sense of complacency about food production. Our staggering requirement for food must be viewed in the context of statistics that indicate that the area available for food production has, essentially, remained constant since 1960 (3). Despite some new land being brought into cultivation, soil erosion and urbanization have offset these gains. In addition, less resources (both human and financial) are being devoted to overcoming major production constraints. Financial support for agricultural research has decreased for the last several years and is expected to continue its slow decline as most developed nations continue to focus on domestic issues rather than addressing the multitude of problems facing the world’s developing nations. How will we feed the world in the coming years? For the foreseeable future, conventional agriculture will be our primary response, with cereal grains playing a pivotal role. The International Food Policy Research Institute has predicted that, by the year 2020, almost 96% of the world’s rice consumption, two-thirds of the world’s wheat consumption, and almost 60% of the world’s maize consumption will be in developing countries. Forecasts call for wheat to surpass rice in its apical role in feeding the poor of those nations. It will likely become the most important cereal in the world, with maize close behind; together, these crops will account for
80% of the cereal import requirements of developing countries. Many economists stress, however, that increased production in developing countries will be essential for achieving food security. Maize and wheat are each expected to have an annual global demand of
775 million tons each † and will be of critical consequence in the race between crop production and population growth. This paper focuses on the potential of genetic resources, particularly those of maize and wheat, to help meet the continually expanding demand for these major grains. It will indicate how such resources have contributed in the past, and how they may advance our efforts in the future.

THE ROLE OF THE CONSULTIVE GROUP ON INTERNATIONAL AGRICULTURAL RESEARCH (CGIAR) IN PRESERVING GENETIC RESOURCES Simply stated, plant breeding depends on the correct combination of specific alleles at the 50–60,000 genetic loci present in a plant’s genome. The knowledge of where these alleles are best found and the combination and evaluation of these into a

* To whom reprint requests should be addressed at: International Maize and Wheat Improvement Center (CIMMYT), Aptdo 370, P.O. Box 60326, Houston, TX 77205. e-mail: [email protected] . † Rosegrant, M. W., Sambilla, M. A., Gerpacio, R. V. & Ringler, C., Illinois World Food and Sustainable Agriculture Program Conference, May 27, 1997, Urbana-Champaign, IL. PNAS is available online at www.pnas.org. Abbreviations: CGIAR, Consultative Group on International Agricultural Research; CIMMYT, Centro International de Mejoramiento de Maiz y Trigo; FAO, Food and Agriculture Organization; IPR, intellectual property rights.

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single species can be considered the “art” of breeding. Obviously, access to a wide range of genetic diversity is critical to the success of any breeding program. The work of the 16 centers that collectively form CGIAR represents the largest concerted effort toward collecting, preserving, and utilizing global agricultural resources. Together, the centers hold nearly 600,000 samples of the estimated 6 million accessions stored globally (Table 1). The remaining germplasm are stored in other international, regional, and national gene banks, many of which collaborate closely with the CGIAR centers. If one considers that the Food and Agriculture Organization (FAO) has estimated that the total number of unique accessions globally are on the order of 1–2 million, the CGIAR centers account for an estimated 30–60% of the world’s unique holdings under long-term conservation. Given that the CGIAR has focused its efforts on the crops of highest significance in world agriculture, this proportion could be even greater. The materials in the CGIAR gene banks include traditional varieties and landraces, nondomesticated species, advanced cultivars, breeding lines, and genetic stocks. The effort required to assemble, document, and maintain these collections is enormous but well justified as the genetic diversity present in the gene banks represents a critical component in the world’s fight against hunger. The International Center for Maize and Wheat Improvement, better known by its Spanish name of Centro Internacional de Mejoramiento de Maiz y Trigo (CIMMYT), has a global mandate for improving the productivity and sustainability of maize and wheat in developing countries. The collection, documentation, and evaluation of the genetic resources of maize and wheat are a critical part of meeting this mandate. CIMMYT’s newly established Genetic Resource Center contains
120,000 accessions of wheat and 18,000 accessions of Latin American maize (of the 25,000–35,000 accessions in partner gene banks in Latin America). This represents the largest collection of these two important cereals. It is, perhaps, the only effort that is actively pursuing the documentation and evaluation of its collection on a routine basis. Before discussing several issues related to the use of these genetic resources, it is important to mention a few examples of their contributions to crop improvement. Although these examples have been drawn mostly from maize and wheat, there are a large number of similar examples for many other major food crops handled by the CGIAR Centers.

Table 1. Summary of CGIAR’s germplasm holdings (4) Total holdings Center CIAT 70,940 CIMMYT 136,637 CIP 13,911 ICRAF 2,448 ICARDA 109,029 ICRISAT 110,478 IITA 39,756 ILRI 13,470 IPGRI 1,051 IRRI 80,646 WARDA 17,440 595,806 Total

Major species Cassava, Phaseolus, rice Maize, wheat Potato, sweet potato Agroforestry species Lentil, chickpea Chickpea, sorghum, groundnut Yam, rice, maize, cassava Forage legumes and grasses Banana, plantain Rice Rice

IITA, Inter national Institute for Tropical Agriculture; CIAT, Centro Internacional de Agricultura Tropical; CIP, Centro Internacional de Papa; ICRAF, International Centre for Research in Agroforestry; ICARDA, International Center for Agriculture in the Dry Areas; ICRISAT, International Crops Research Institute for the Semi-Arid Tropics; ILRI, International Livestock Research Institute; IPGRI, International Plant Genetic Resources Institute; IRRI, International Rice Research Institute; WARDA, West African Rice Development Association. IITA, Inter national Institute for Tropical Agriculture; CIAT, Centro Internacional de Agricultura Tropical; CIP, Centro Internacional de Papa; ICRAF, International Centre for Research in Agroforestry; ICARDA, International Center for Agriculture in the Dry Areas; ICRISAT, International Crops Research Institute for the Semi-Arid Tropics; ILRI, International Livestock Research Institute; IPGRI, International Plant Genetic Resources Institute; IRRI, International Rice Research Institute; WARDA, West African Rice Development Association.

CONTRIBUTIONS OF WHEAT GENETIC RESOURCES Wheat is truly global, being one of the few crops grown over most of the world. It belongs to the genus Triticum, which originated almost 10,000 years ago in the historic Fertile Crescent, an area in the Middle East. Triticum arose from the cross (supposedly in nature) of two diploid wild grasses to produce tetraploid wheat, which today includes the many cultivated durum (pasta or macaroni) wheats (Triticum turgidum L. var. Group durum Desf. 2n = 4x = 28). Tetraploid wheat later crossed to diploid goat grass (Triticum tauschii) and gave rise to hexaploid, or bread wheat (Triticum aestivum L. em Thell. 2n = 6x = 42). There are hundreds of thousands of wild species, landraces, and local cultivars within the Triticum species that constitute the wheats of the world. The main center of diversity of the species is southwest Asia, near the Fertile Crescent, extending from the Mediterranean coast in the west to the Tigris-Euphrates plain in the east. In this region, diploid and polyploid Triticum species coexist in mixed populations and exhibit tremendous morphological and ecological diversity. Thousands of species of Triticum have been collected and are currently stored in the various genetic resources centers, including the one at CIMMYT headquarters in Mexico. Much has been written about the lack of utility of genetic resources contained in collections, but few studies have attempted to estimate their contribution to wheat improvement. Chapman (5) examined the role of genetic resources (defined as wild materials and landraces) in wheat breeding, but found it difficult to estimate. He concluded that these materials may have been used in
10% of all crosses based on the pedigrees of recently released cultivars. CIMMYT’s effort to develop a full pedigree database of the global wheat genetic resources (the International Wheat Information System) allows a more complete estimate of landrace and wild material contributions to modern varieties by providing pedigree information that goes back to the original landrace parents. More recently, Smale (6) performed an indepth analysis of the use of wheat genetic resources and the international flow of wheat genetic resources. The study found that the number of different landraces in pedigrees of modern wheat varieties has steadily increased during the past 30 years and that the geographical origin of the landraces has broadened. Going beyond rather general and poorly defined contributions to modern varieties, several specific genes that have made major impacts on wheats can be directly traced to contributions from genetic resources. Dwarfing Genes. “Norin 10,” a cultivar from Japan, provided two very important genes, Rht1 and Rht2, that resulted in the reduced height (or dwarf) wheats. Norin 10, in turn, inherited these genes originally from “Shiro Daruma,” a Japanese landrace (7). When Norman Borlaug first arrived in Mexico under the joint Rockefeller/Mexico project, wheat productivity was extremely low. The tall varieties being planted were prone to lodging and would not respond to added fertilizer inputs. Borlaug speculated that, by reducing the height of the wheat plant, it would suffer less lodging even under the higher input levels. The incorporation of the Rht1 and Rht2 genes into the new varieties that Borlaug ultimately was able to develop and deploy illustrated the difficulty of using genes from unadapted materials. But more importantly, it led to what is now been termed the “Green Revolution” (8, 9). While it was originally thought that these genes contributed to higher production simply through reduced lodging via reduced height, it is now clear that they have other direct effects on yield via better nutrient uptake and tillering capacity (8, 10).

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Rust Resistance. Some of the most devastating and universal crop diseases are caused by fungal pathogens. Among them, the rust pathogens are the most widespread and generally cause the largest crop losses per season. Many genes have been found that provide resistance to specific races of each rust pathogen. Within wheat, leaf, yellow, and stem rusts are major pathogens. Fungicides can provide a level of control; however, the chemical option is often limited for many farmers, particularly in developing countries, by high costs and lack of knowledge about application. In addition, the negative environmental effects of chemical applications can be considerable. The incorporation of host plant resistance genes into modern wheat varieties has allowed yields of resistant wheat that have not been treated with fungicides to nearly equal those of the same varieties under fungicide applications (6). Many of these varieties have incorporated single major genes that convey resistance to specific races of the rust pathogen. Of >40 known genes for leaf rust resistance, 12 originated in species other than T. aestivum and T. turgidum while 20 of the 41 known genes for stem rust resistance originated in species other than T. aestivum and T. turgidum (ref. 11 ; also see Table 2). Even among the genes originating from T. aestivum, many come from landraces. Unfortunately, many of these major genes have already been “broken”; i.e., the specific race has mutated to become virulent against the specific resistance gene. Efforts to identify and incorporate genes that confer “durable” resistance are therefore preferable. Several such genes have been identified and incorporated into modern wheat varieties. One of the most important is Lr34, which was originally found in the cultivar “Frontana” (13). Lr34 has been incorporated into >50% of the wheat varieties grown in the world today; together with several modifier genes, it has resulted in stable resistance to leaf rust in the 1980s and 1990s. Most of these durable sources of resistance have not come from alien sources but from cultivars and landraces that evolved in the past to contain broad levels of resistance to pathogens.

Table 2. Important genes in wheat that were found in related species (12) Locus Trait Disease resistance Leaf rust Lr9 Lr18 Lr19 Lr23 Lr24 Lr25 Lr29 Lr32 Stem rust Sr2 Sr22 Sr36 Stripe rust Yr15 Powdery mildew Pm12 Pm21 Pm25 Wheat streak mosaic virus Wsm1 Karnal bunt Qqantitative trait loci Pest resistance Hessian fly H21 H23, H24 H27 Cereal cyst nematode Cre3 (Ccn-D1) Quality traits Grain protein Quantitative trait loci High protein Low molecular weight glutenins

Source Aegilops umbellulata Triticum timopheevi Thinopyrum T. turgidum Ag. elongatum Secale cereale Ag. elongatum T. tauschii T. turgidum Triticum monococcum Triticum timopheevii Triticum dicoccoides Aegilops speltoides Haynaldia villosa T. monococcum Ag. elongatum T. turgidum S. cereale T. tauschii Aegilops ventricosa T. tauschii T. turgidum T. dicoccoides T. turgidum

The cultivar “Hope,” bred in the United States earlier in the century (14), was later used by Borlaug as a source of stem rust resistance in the Rockefeller/Mexico wheat program. The Hope resistance was based on the Sr2 gene that, when combined with other unidentified genes, produced a more durable resistance. The Sr2 originally came from a tetraploid wheat variety known as emmer and has since been incorporated into many wheat varieties worldwide, providing excellent levels of resistance. Recently, a linked molecular marker was developed (15) that may allow more rapid identification and manipulation of this important gene. It is fair to say that the incorporation of the Sr2 and Lr34 genes from genetic resources into cultivated wheat varieties represent milestones in the grain’s genetic advancement. Most likely, the gains of the Green Revolution could not have been made without them. Veery Wheats. Genetic resources have contributed more than single genes to crop improvement efforts; entire chromosomal segments also have been introduced with noteworthy results. Perhaps the most important of these is the 1B/1R translocation that was identified as a simple transfer between rye and wheat in the former Soviet Union cultivar “Kaukaz.” The 1B/1R translocation, which carries a number of genes from rye, confers resistance to various diseases (fungal and viral pathogens) and adaptation to marginal environments (16). This translocation has been deemed so important that it has been incorporated into >60 wheat varieties, including the prominent Veery lines, that occupy >50% of all developing country wheat area, almost 40 million hectares (17). Yield Potential. Yields of the major cereal crops (rice, wheat, and maize) have increased steadily over the past years, although the rate of these yield increases appears to have slowed. ‡ To meet cereal production demand in the next decade, we must continue to increase yields; even more daunting, we must increase them at an ever-increasing rate. How will such growth be supported, particularly when the rates of increase over the past few years appear to have declined? For rice and wheat, the use of hybrids may be one possibility, although it remains to be demonstrated what level of heterosis (hybrid vigor) can be achieved in either crop. Heterosis levels currently detected in wheat are
10–25%, lower than the 25–35% levels historically found in maize, one of the first hybrid cereal crops. The reasons for wheat’s lower heterosis levels have not been determined, but one possibility is the lower level of diversity generally found in self-pollinated crops such as rice and wheat. Many groups continue to search for alternatives to the existing germplasm. In wheat, it is possible to reproduce the hybridization event that created hexaploid wheats from a cross of tetraploid with diploid wheat. These so-called “synthetics” represent a source of novel genetic variation (18). Research at CIMMYT has led to the development of >600 new synthetic wheats, crosses between various durum wheats and T. tauschii accessions. Many of these crosses have produced rapid improvements in important characteristics, including disease resistance, abiotic stress tolerance, and yield. Although much work remains to be done, the use of molecular genetic techniques now allows us to identify the gene segments most likely responsible for improved performance and, thus, to focus on more directed crosses in the future. A recent example, now under investigation at CIMMYT, is the role of the Lr19-containing segment. This gene (or segment) originally came from Agropyron elongatum and was

‡ Rosegrant, M. W., Sambilla, M. A., Gerpacio, R. V. & Ringler, C., Illinois World Food and Sustainable Agriculture Program Conference, May 27, 1997, Urbana-Champaign, IL.

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first incorporated into the wheat variety “Agatha” (11). Yield trial data indicates that varieties containing the Lr19 gene yield at least 10% more than counterparts without Lr19 (Ravi Singh, personal communication). The gene was originally transferred for its possible role in conferring leaf rust resistance, but its potential to increase yields may become a more important factor for breeders, thus demonstrating the often unanticipated potential of these alien transfers.

USE OF GENETIC RESOURCES IN MAIZE IMPROVEMENT Unlike wheat, the use of genetic resources in maize improvement has not been well documented at the global level and may not be as great. Although
50,000 accessions of maize exist in germplasm banks around the world (19, 20), most of these have never been adequately evaluated for useful traits. Reasons cited for low utilization include lack of evaluation data, documentation, and information; poor coordination of national policies; and poor linkages between gene banks and breeders (21). The untapped potential of these genetic resources is indicated to some extent by the progress that U.S. breeders achieved through a combination of plant improvement and pedigree breeding. Using double and three-way crosses, varieties were produced that helped double U.S. yields between 1930 and 1966; by 1995, single crosses and the use of better hybrid materials by breeders helped triple 1930 yields. Meanwhile, there have been frequent warnings about the genetic vulnerability of maize and the potential of exotic germplasm to reduce the threat (22–24). It has been estimated that, in the U.S., 60°). Subtropical and tropical regions will experience less extreme temperature changes. Monsoon rains are likely to penetrate further northward. Northern areas in which production is presently constrained by length of the growing season, such as the northern fringes of the Canadian prairie provinces, could expect both higher yields and an expansion of area devoted to cereals and forage plants. There has been a substantial change in estimates of the impact of global climate change on crop yield and agricultural production. Estimates made in the late 1980s and early 1990s generally projected rather substantial negative impacts at the global level (53). More recent studies have tended to project impacts ranging from slightly negative to slightly positive (55, 56). These more positive estimates have been due primarily to two changes in the modeling of climate change. One has been the incorporation of assumptions about the positive effects of CO2 fertilization. As noted above, these assumptions remain controversial because they involve extrapolation from greenhouse or very small scale field experiments. The second change has been due to replacing the static production function or “dumb farmer” approach employed in earlier models with estimates of farmers’ rational responses to climate change, including changing in cropping systems and adoption of technology. As a caveat, several of the models suggest that, while modest changes in global average surface temperature in the 2.5° range, for example, could have a net positive effect, larger increases, in the 5° range, could have a negative effect on agricultural production. l The modeling efforts continue, however to employ a “dumb scientist” assumption. The behavior of public and private sector suppliers of knowledge and technology has not yet been incorporated in the models and estimates. Efforts to incorporate endogenous or induced technical change into climate change models have been limited by the tractability of the models (or the modelers). The only successful empirical effort I am aware of is a study by Evenson and Alves in Brazil (57). The Evenson-Alves model incorporates not only the choice of technology by farmers in response to climate change but also responses by the public and private suppliers of technology. The study indicates that, in Brazil, the effect of climate change alone would be to depress production in the North, Northeast, and Center-West. In contrast, many areas in the Center-East, the South, and the Coastal regions would benefit. When the technical change induced by the climate change is taken into account, it is expected to compensate for the effect of climate change in the more disadvantaged regions while the more favored regions will benefit from both the climate change and technical change. None of the models gives adequate attention to the indirect or interactive effects of climate change. The limited assessments that have been made suggest that, as environmental stress intensifies as a result of warmer (and, in some areas, more humid) climates, crops will become more vulnerable to weeds, insects, and plant diseases (54). The incidence and severity of soil erosion, changes in rainfall, surface water storage, groundwater recharge, the incidence of pests and pathogens, or frequencies of extreme events, such as drought or floods, or climate variability have not been incorporated effectively into the climatic change models. It is possible that actions taken to mitigate global climate change, such as land-intensive approaches to carbon sequestering, substitution of fuels based on agricultural raw materials for petroleum based fuels, and efforts to control carbon, nitrous oxide, and methane emissions, could have a larger negative effect of crop and animal production than the direct impacts of climate change. I have not, in this paper, discussed the potential impacts of health constraints on agricultural production. Improvements in nutrition associated with growth in agricultural production has, in many developing countries, contributed to lower infant mortality and increased life expectancy. But the increase in use of insecticides and herbicides associated with agricultural intensification has also had negative effects on the health of agricultural workers. There are also important health effects, in both urban and rural areas, of the intensification of industrial production associated with atmospheric, water, and soil pollution. There are also the health effects associated with the emergence of new diseases such as AIDS and the emergence of drug resistance by older parasitic and infectious diseases. It is not too difficult to visualize situations in particular villages in which the coincidence of several of these health factors could result in serious threats to agricultural production. It is more difficult, but not completely impossible, to visualize health threats becoming a serious constraint on national agricultural production (60–62).

PERSPECTIVE What inferences do I draw from this review of resource and environmental constraints on the transition to agricultural

l The Mendelson, Nordhaus, and Shaw model (55) has also been criticized for underestimating the impact of global climate change on agriculture in irrigated areas by giving inadequate attention to the way water is currently used due to distortions associated with water allocation and pricing (58).

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sustainability? There will, even beyond the middle of the 21st century, continue to be great diversity among countries and regions in the transition to agricultural sustainability. It seems unlikely that the conditions projected in the Barbarization Scenario will be completely eliminated or that the conditions projected in the New Sustainability Scenario will be more than partially realized (Fig. 1). It is unlikely that soil loss and degradation will represent a serious constraint on global agricultural production over the next half-century. But soil loss or degradation could become a serious constraint on production on a local or regional scale in some fragile resource areas. This possibility will be greatest if slow productivity growth in robust resource areas should lead to intensification or expansion of crop and animal production in fragile resource areas, i.e., tropical rain forests, arid and semiarid regions, and the high mountain areas. In some such areas, however, the possibility of sustainable production can be enhanced by irrigation, terracing, careful soil management, and changes in commodity mix and farming systems. It is also unlikely that lack of water resources will become a severe constraint on global agricultural production in the foreseeable future. But in 50–60 of the world’s most arid countries, plus major regions in several other countries, competition from household, industrial, and environmental demands will result in a reallocation of water away from irrigation. In many of these countries, increases in water use efficiency and changes in farming systems will permit continued increases in agricultural production. But it seems reasonable to expect that, in a number of countries, the reduction in irrigated area will be large enough to result in significant reductions in agricultural production. Since these countries are among the world’s poorest, some may have great difficulty in meeting food security needs from either domestic production or food imports. The problem of pest and pathogen control may have more serious implications for sustainable growth in agricultural production at a global level than either land or water constraints. Both the development of resistant crop varieties and chemical methods of control tend to induce target pest or pathogen resistance. In addition, international travel and trade will result in rapid diffusion of traditional and newly emerging pests and pathogens to favorable environments. As a result, new pest control technologies must constantly be replaced by a succession of resistant varieties and chemical (or biochemical) agents. As a result, an increasing share of a constant research budget will need to be devoted to maintenance research—the research required to sustain existing productivity levels. Recent projections of the impact of climate change on global agricultural production are much more optimistic than projections made a decade ago. The scientific and empirical basis for the more optimistic projections is, however, much too fragile to serve as a secure foundation for policy. There is great uncertainty about the rate of climate change that can be expected over the next half-century. All of the projections employ assumptions that are only weakly grounded in experience. None of the models gives adequate attention to the synergistic interactions among climate change, soil loss and degradation, ground and surface water storage, and the incidence of pests and pathogens. These interactive effects could add up to a significantly larger burden on sustainable growth in production than the relatively small effects of each constraint considered separately. A point made repeatedly in this paper is that, while the constraints discussed do not represent a threat to global food security, they may, individually or collectively, become a threat to growth of agricultural production at the regional and local level in a number of the world’s poorest countries. This means that the transition to agricultural sustainability will, given the uncertain future, depend on the maintenance and enhancement of capacity for technical and institutional innovation. A primary defense against the uncertainty about resource and environmental constraints is agricultural research capacity. Research capacity represents the “reserve army” to deal with uncertainty. The erosion of capacity of the international agricultural research system will have to be reversed; capacity in the presently developed countries will have to be at least maintained; and capacity in the larger developing countries will have to substantially strengthened. Smaller countries will need, at the very least, to strengthen their capacity to borrow, adapt, and diffuse technology from countries in comparable agroclimatic regions. It also means that more secure bridges must be built between the “island empires” of agriculture, environment, and health. If the world fails to meet the challenge of a transition to sustainable growth in agricultural production, the failure will be at least as much in the area of institutional innovation as in the area of resource and environmental constraints. This is not an optimistic conclusion. The design of institutions capable of achieving compatibility between individual, organizational, and social objectives remains an art rather than a science, The incentive compatibility problem has not been solved analytically, even at the most abstract theoretical level (63, 64). At our present stage of knowledge, institutional design is analogous to driving down a four-lane highway looking out of the rear view mirror. 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20. Pimentel, D. , Terhune, E. C. , Hudson, R. D. , Rochester, S. , Sarris, R. , Smith, E. A. , Denman, D. , Reitschneider, D. & Sheperd, M. (1976) Science 194, 149–154 . 21. Daily, G. C. , Matson, P. A. & Vitousek, P. M. (1995) in Natual Services: Societal Dependence on Natural Ecosystems (Island , Washington, DC), pp. 113–132 . 22. Pimentel, D. , Harvey, C. , Resosudarmo, P. , Sinclair, K. , Kurtz, D. , McNair, M. , Crist, S. , Shpritz, L. , Fitton, L. , Saffouri, R. , et al. (1995a) Science 267, 1117–1123 . 23. Harris, J. M. (1990) World Agriculture and the Environment (Garland , New York ), p. 115 . 24. Crosson, P. (1995) “Soil Erosion and its On-Farm Productivity Consequences: What Do We Know?” Washington, DC : Resources for the Future Discussion Paper 95–29 . 25. Crosson, P. (1995b) Science 269, 461–463 . 26. Pimentel, D. , Harvey, C. , Resosudarmo, P. , Sinclair, K. , Kurtz, D. , McNair, M. , Crist, S. , Shpritz, L. , Fitton, L. , Saffouri, R. , et al. (1995) Science 269, 464–465 . 27. Lal, R. (1984) in Quantification of the Effect of Erosion on Soil Productivity in an International Context, eds. Rijsberman, F. & Wolman, M. (Delft Hydraulics Lab. , Delft, The Netherlands), pp. 70–94 . 28. Anderson, J. R. & Thompapillia, J. (1990) Soil Conservation in Developing Countries: Project and Policy Interaction (World Bank , Washington, DC). 29. Lindert, P. H. (1996) in Agricultural Science Policy: Changing Global Agendas, eds. Alston, J. & Pardy, P. (Department of Natural Resources and Environment , Melbourne, Australia), pp. 263–332 . 30. Lindert, P. H. (1999) Econ. Dev. Cultural Change, in press . 31. Lindert, P. H. (1998) A Half Century of Soil Change in Indonesia (Univ. of California Agricultural History Center , Davis, CA). 32. National Research Council (1993) Sustainable Agriculture and the Environment in the Humid Tropics (National Academy Press , Washington, DC). 33. Seckler, D. , Molden, D. & Barker, R. (1999) Int. J. 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(1991) Unwelcome Harvest: Agriculture and Pollution (Earthscan Publications , London). 49. Curtis, J. , Mott, L. & Kuhnle, T. (1991) Harvest of Hope: The Potential for Alternative Agriculture to Reduce Pesticide Use (Natural Resources Defense Council , Washington, DC). 50. Pimentel, D. , McLaughlin, L. , Zepp, A. , Lakitan, B. , Kraus, T. , Kleinman, D. , Vancini, F. , Roach, W. J. , Graap, E. , Keeton, W. , et al. (1991) in Handbook of Pest Management in Agriculture, ed. Pimentel, D. (CRC , Boca Raton, FL). 51. Gianessi, L. P. (1991) “Reducing Pesticide Use with no Loss in Yields? A Critique of a Recent Cornell Report.” Washington, DC : Resources for the Future Discussion Paper QE91–16 . 52. Clark, W. L. & Munn, R. E. , eds. (1989) Sustainable Development of the Biosphere ( Cambridge Univ. Press , Cambridge, U.K. ). 53. Parry, M. L. (1990) Climate Change and World Agriculture ( Earthscan Publications , London). 54. Rosenzweig, C. & Hillel, D. (1998) Climate Change and the Global Harvest (Oxford Univ. Press , New York). 55. Mendelsohn, R. , Nordhaus, W. D. & Shaw, D. (1994) Am. Econ. Rev. 84, 753–771 . 56. Adams, R. M. , Hurd, B. , Lenhart, S. & Leary, N. (1999) J. Climate Res., in press . 57. Evenson, R. E. (1988) “Technology, Climate Change, Productivity and Land Use in Brazilian Agriculture.” New Haven, CT : Yale University Economic Growth Center Staff Paper . 58. Fischer, A. & Hannenan, M. (1998) “The Impact of Global Warming on Agricultural Production: A Rethinking of the Ricardian Approach.” Berkeley, CA : Dept. of Agricultural and Resource Economics, University of California , Working Paper 842 . 59. Sinclair, K. (1999) Proc. Natl. Acad. Sci. USA, in press . 60. Lederberg, J. (1996) J. Am. Med. Assoc. 276, 412–419 . 61. Ruttan, V. W. , ed. (1994) Health and Sustainable Agricultural Development Westview Press , (Boulder, CO) . 62. Pimentel, D. , Tort, M. , D’Anna, L. , Krawick, A. , Berger, J. , Rossman, J. , Mungo F. , Doon, N. , Shriberg, M. , Howad, E. , et al. (1998) Bioscience 48, 317–326 . 63. Hurwicz, L. (1973) Am. Econ. Rev. 63, 1–30 . 64. Hurwicz, L. (1998) in Designing Institutions for Environmental Resource Management, eds. Loehman, E. T. & Kilgour, D. M. (Edward Elgar , Cheltenham, U.K.). 65. Johnson, G. (1999) Proc. Natl. Acad. Sci. USA 96, 5915–5920 . 66. Cassman, K. G. (1999) Proc. Natl. Acad. Sci. USA 96, 5952–5959 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Biotechnology: Enhancing human nutrition in developing and developed worlds

GANESH M. KISHORE * AND CHRISTINE SHEWMAKER Nutrition and Consumer Products, Monsanto Company, 800 North Lindbergh, St. Louis, MO 63167 ABSTRACT While the last 50 years of agriculture have focused on meeting the food, feed, and fiber needs of humans, the challenges for the next 50 years go far beyond simply addressing the needs of an ever-growing global population. In addition to producing more food, agriculture will have to deal with declining resources like water and arable land, need to enhance nutrient density of crops, and achieve these and other goals in a way that does not degrade the environment. Biotechnology and other emerging life sciences technologies offer valuable tools to help meet these multidimensional challenges. This paper explores the possibilities afforded through biotechnology in providing improved agronomic “input” traits, differentiated crops that impart more desirable “output” traits, and using plants as green factories to fortify foods with valuable nutrients naturally rather than externally during food processing. The concept of leveraging agriculture as green factories is expected to have tremendous positive implications for harnessing solar energy to meet fiber and fuel needs as well. Widespread adaptation of biotech-derived products of agriculture should lay the foundation for transformation of our society from a production-driven system to a quality and utility-enhanced system. Over the last 50 years, our society has faced the challenge of feeding an ever-growing world population. Human population has literally doubled in the last 40 years and increased 6-fold in the last 200 years. Since the beginning of this century, agriculture has intensified—first, with the discovery of economic, chemical processes to reduce nitrogen to ammonia and the use of nitrogenous fertilizers in agriculture, superior genetics with hybrid as well as varietal crops, resulting in a global green revolution, and finally, with the discovery and use of chemical pesticides to manage a range of pests, including weeds, microbes, and insects. Intensive agriculture as practiced today fully leverages all of the above advances and in addition is benefited by superior irrigation techniques, better tillage systems, etc. Global cereal yields practically doubled between 1960 and 1990. Yields of both rice and wheat, crops largely consumed by the rapidly growing Asian population, have dramatically increased. These agricultural technologies, however, have not kept pace with projected population increases. If population outstrips food availability, more marginal land will necessarily be placed into agricultural use, heavier inputs will be applied, and food self-sufficiency, especially in emerging economies, will be compromised. The challenge over the next 50 years will be to not only feed more people, but to do so in such a way that takes into account these facts: • There will be less arable land. A combination of overplowing, overgrazing, and deforestation has caused soil erosion to exceed soil formation. Countries particularly hard hit are those in continents like Africa, where soil is shallow to begin with. The next generation of farmers in Africa will need to feed not the 719 million people of today, but 1.45 billion people in the year 2025 and with far less topsoil (1). Even so-called low-tech agriculture, sometimes viewed as more sustainable, still relies on chemical inputs and involves techniques, such as plowing, that degrade the soil. • There will be fewer resources, particularly nonrenewable resources like phosphorus and potassium, which go into fertilizers. The U.S. Bureau of Mines showed a 7-fold increase in consumption of U.S. industrial minerals, including fertilizers and feed stocks from 1900 to 1980, and this trend is expected to continue (2). While it could be argued that we have sufficient natural deposits of these minerals to last another 200 years, technologies that minimize ore extraction and dispersion over vast areas of land will enhance the sustainability of our agricultural systems. • There will be less water, and the quality of remaining water also will be reduced as demand increases. Also, competition for reduced water supplies between rural and urban societies will increase. Water use has tripled since midcentury (3), and water tables are falling all around the world. Seventy percent of all the water pumped from underground or drawn from rivers is used for irrigation, and if we face a future of water scarcity, we also face a future of food scarcity. • Fewer people will be engaged in primary agriculture in both developed and developing countries. In the United States, less than 1% of the population is engaged in primary agriculture, compared with 60% of the population in the early 1900s (U.S. Bureau of the Census). • People engaging in primary agriculture will be older. The breadbaskets of the world, particularly Western Europe and North America, have the most graying population. The generation born in the U.S. during the baby boom of the 1950s will be in their 60s by 2010, ushering in an age of unparalleled increase in absolute numbers of elderly. According to the U.S. Bureau of the Census, by 2010, half of the U.S. population will be 37 or older—a very high median age (4). This aging society will need technologies that will allow it to produce food in a more cost-effective, less labor-intensive, and more convenient way than they have done in the past. • Health-care costs will continue to increase as the population ages, putting more demands on public aid. Governments’ ability to pay for Social Security and health care will decline as the population increases and the number of people contributing to Social Security, once the baby-boom generation retires, will decrease. This will be particularly critical for the developed nations of this planet. For the developing economies, health care oriented toward prevention and

*To

whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org.

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health delivered inexpensively is critical as their middle class expands and human longevity dramatically increases. • As a result, food that can provide more than just calories and essential nutrients but has the ability to delay the onset of degenerative diseases and aging will be a powerful contributor to a healthy, global society. We need an array of new and improved technologies, which can form the foundation for infrastructure and cultural improvements, to help address these challenges. Luckily, we are entering an epoch rich with opportunity for breakthrough technologies. Termed the information revolution, this era is certain to have at least as big an impact on society as the agricultural revolution and the industrial revolution. Information-driven agriculture will have two components. The first is information based on genomics, the study of genes, the strands of life, which is an enabling link across life sciences, including agriculture, food and nutrition, and pharmaceuticals. This constitutes the next tier in scientific understanding and opportunity and is discussed in greater detail later. The second component is information that is based on the silicon revolution of the present time. Computer and modern electronic communication systems can be applied across the life sciences to maximize value. Today, in agriculture, farmers are taking advantage of the system for precision agriculture that optimizes inputs, characterization of outputs so that they can match the needs of their customers with specific products as well as managing their business based on real-time information. Biotechnology is a discipline that has developed rapidly during the last two decades. This technology is based on our fundamental ability to precisely introduce genetic changes into an organism. Plant biotechnology in particular has evolved rapidly over the course of the last 15 years. Every major crop can be subject to precise genetic modifications based on our ability to introduce and express genes in crops. Plant biotechnology therefore should substantially augment plant breeding, which in many respects was based on our ability to harness genes into plants either by sexual crossing or laboratory techniques such as cell fusion. We anticipate that plant biotechnology will go through three phases of development, creating significant value at each stage. The first is agronomic trait development, the second is differentiated crop development, and the third is use of plants as factories. These are discussed in detail below.

AGRONOMIC TRAITS Since 1995, major products with improved agronomic traits have been introduced in the U.S. and other parts of the world. These are mostly single gene traits where a single gene has had a dramatic positive impact on grower productivity. This is reflected in the widespread acceptance and use of genetically improved crops in the United States, which is estimated to be 46 million acres. A few examples of these products are Monsanto’s Roundup Ready soybeans and YieldGard corn and are discussed below. Roundup Ready soybeans contain a gene encoding the enzyme 5-enolpyruvylshikimate 3-phosphate synthase (EPSPS) involved in the biosynthesis of aromatic amino acids in plants. The EPSPS gene naturally present in soybeans produces a form of the enzyme sensitive to glyphosate, the active ingredient of Roundup, whereas the gene in Roundup Ready soybeans encodes a catalytically active and glyphosatetolerant form of the same enzyme (5). Expression of this gene in plants renders adequate commercial tolerance to this herbicide. Roundup Ready soybeans are one of the most widely accepted products that have been introduced in the history of agriculture. Within 3 years of commercialization, the crop has grown to the point where it now accounts for almost 40% of total U.S. soybean acreage. Roundup Ready soybeans offer several benefits to farmers, including a superior weed management system. Roundup, a post-emergent, broad spectrum herbicide controls most weeds in the field and needs to be used only when weed control is needed. Indeed in 1997, U.S. growers used only Roundup on 83% of the Roundup Ready soybean acres. Another benefit is yield optimization (5% higher yield with lower operating costs). Roundup also has demonstrated favorable environmental characteristics. It breaks down over time in soil to innocuous products (ammonia, phosphate, carbon dioxide and water), is highly unlikely to move in groundwater, does not accumulate in the environment or food chain, and is practically nontoxic to multiple life forms such as aquatic, avian, animal, and human. The combination of the Roundup Ready soybeans and Roundup also enhances the ability of the farmer to use the seeds in conjunction with less resource-intensive farming practices like conservation tillage, which helps conserve topsoil. Before the introduction of this product into the marketplace, we conducted a number of safety assessments for not only the herbicide but also the genetically improved soybeans. Those studies demonstrated the nutritional equivalency of the soybeans containing the Roundup Ready gene to those without the gene. The gene product also was investigated for its safety and digestibility and demonstrated to be a rapidly digested protein similar to many other proteins found in our food chain (6). YieldGard corn uses a plant-modified version of the gene encoding an insecticidal protein from a naturally occurring bacterium, Bacillus thuringiensis (7, 8) to help the plant resist the European corn borer, which annually infests some 40 million acres of crops in the U.S. Average annual yield loss caused by the corn borer is 6% and can be as high as 20% and represents $1–2 billion in losses to farmers depending on the extent of infestation of the corn borer. With YieldGard, farmers achieve 11–15 additional bushels of corn per acre. Even subclinical infestations, which otherwise would go untreated resulting in smaller yields, can be avoided, thereby boosting yields. The YieldGard gene significantly reduces the damage caused by the European corn borer to the corn crop—damage that has the potential to cause onset and spread of fungi and other microbes in the corn plant and produce undesirable toxins. Safeguarding the corn plant against the corn borer therefore provides secondary benefits of yield protection from other pests as well as quality protection. While our discussion above has been restricted to two examples of products of biotechnology, it should be pointed out that several other products within the category of agronomic traits have been introduced into the marketplace. These include Bollgard cotton, Roundup Ready canola, cotton, and corn, Liberty Link canola and corn, New Leaf potato, virus-resistant squashes, and melons. Near term, a number of other agronomic traits are expected to be commercialized. In our own laboratories at Monsanto, we are working on a trait that will protect corn from corn root worm, a major insect pest of corn that causes losses approaching $1 billion in the U.S. Healthy root systems, crucial for water and fertilizer uptake, are destroyed by this pest. By controlling root worm, it is our expectation that not only is the yield likely to be better protected but the crop also will have greater drought tolerance and fertilizer use efficiency, leading to better grain quality. Resistance against head scab disease in wheat, caused by the fungus Fusarium graminareum, is another agronomic trait under development. Longer-term agronomic traits such as crop architecture redesign, better fertilizer utilization, heat, frost, and drought resistance, as well as salinity and heavy metal tolerances are expected to be developed. Understanding the functions of many of the genes in plants will be critical for

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these advances to occur. Plant genomics will play a pivotal role in this endeavor.

DIFFERENTIATED CROPS While agronomic traits discussed in the previous section have largely focused on input traits, differentiated crops are more focused on grain quality or output traits. Classical breeding has produced a diverse array of differentiated crops such as canola vs. high erucic and glucosinolate containing rape; waxy and high amylose maize vs. yellow dent corn; basmati vs. long grain rice; durrum wheat vs. regular wheat, etc. With biotechnology, our ability to create differentiated, value-added products that create value downstream of production is greatly enhanced. Such differentiated crop offerings are beginning to appear in the marketplace and are discussed below. A vast majority of the grains in the Western Hemisphere are used for feeding animals, and it is not surprising that a significant activity in the differentiated crop arena is focused on improving the feed quality of crops. Two types of products now are being created—one focused on increasing caloric density of the grain by increasing its oil content and another on nutrient density, particularly the levels of protein, essential amino acids, and other micronutrients. High-oil corn, introduced by DuPont, is the first example of this type of product. High-oil corn typically has an oil content of more than 6% as opposed to the 3–4% found in commodity corn. This near doubling of the oil content is expected to dramatically reduce the exogenous addition of fats in the diets of animals and birds. One of the major problems with high-oil corn germplasm has been the yield drag associated with the product. This has been substantially addressed by a technique known as TopCross. Although high-oil corn is not strictly a biotechnology product of the type described earlier for agronomic traits, molecular aspects of breeding have facilitated the rapid creation and commercialization of the product. Our understanding of the genome of corn and other cereals should facilitate molecular breeding and harness the genomic potential of these crops much more powerfully in the future. High-oil corn now is being improved by the addition of high-protein genes as well as by increasing the essential amino acid content of the grains. The high-protein trait itself is also a product of molecular breeding, while high lysine is derived by introduction of critical genes altering the flux of carbon and nitrogen via the lysine pathway in the seed. In the future, we should expect cereals fortified with all the critical essential amino acids such as lysine, methionine, threonine, and tryptophan, and thus be able to reduce the exogenous applications of these amino acids in feed rations. In addition to corn, other crops such as wheat, soybeans, and canola are being subjected to similar improvements. Direct utilization of the grain by improvements in nutrient density and taste/texture appeal for human consumption will go a long way toward meeting not only the food demands of our ever-growing population but also indirectly will benefit our society by increasing the levels of phytonutrients, which are being increasingly shown to have health-promoting attributes in humans (9, 10). Our research efforts have focused on oil modification of canola and soybeans. Most of the oil derived from oil seeds is used in human consumption. Vegetable oils generally are preferred to oils and fats from other sources because of their higher content of mono- and polyunsaturated fats. Fats and oils are one of the most important flavor and texturizing components of food. To create the appropriate texture and mouth feel in foods, it is often necessary to hydrogenate vegetable oils, a process that results in the production of trans-fatty acids. There is a growing body of evidence that suggests that trans-fatty acids found in hydrogenated fatty acids may potentially increase total and low density lipoprotein (LDL) cholesterol in humans. Total and LDL cholesterol now are widely accepted as some of the important biomarkers of the risk of cardiovascular disease in humans, and a number of countries are making significant efforts to educate people on the benefits of keeping the levels of these two biomarkers in the healthy range (National Cholesterol Education Program). By inhibiting the conversion of stearate to oleate in plants, it is possible to produce a trans-fatty acid-free solid or semi-solid fat directly in oilseeds. One of the advantages of stearate over other saturated fatty acids is that it is not hypercholesteremic (11). High stearate soybean and canola now have been produced and are being evaluated for their commercial utility. Grain legumes are some of the most valuable sources of vegetable protein in the human food and feed chain. Soybean, a legume grown on a majority of the legume acreage of the world, is a vital protein source for many people living in Asia. Its use as a protein source can be further enhanced if several attributes such as flatulence, beany flavor, texture, and emulsification properties can be addressed. A number of laboratories are attempting to address these issues.

PLANTS AS FACTORIES Plants, nature’s best manufacturing system, provided the sole source of food, feed, and fiber to society for many centuries until fossil fuel use began. The concept of using plants in place of chemical or nutrient factories to supply food, feed, and fiber is gaining significant attention and constitutes the first step toward biotech-based, nutritionally fortified foods. An important example is high carotenoid canola, rich in beta carotene—a precursor to vitamin A. Many of the western countries address the problem of vitamin A needs of humans by fortifying milk with this vitamin. However, this system is impractical in most parts of the world. According to WHO (12), vitamin A deficiency is today a global epidemic—250 million children are at risk of vitamin A deficiency on an annual basis, and somewhere around 10 million people suffer from significant illness and death resulting from a vitamin A deficiency in their diets. This deficiency results in impairment of vision, protein malnutrition (vitamin A affects amino acid absorption and utilization), and impairment of immune functions. Essentially all countries in Latin America, Asia, and Africa are either clinically or subclinically deficient in vitamin A (13, 14). The best sources of vitamin A are the carotenes, particularly beta carotene, found in many fruits and vegetables. These carotenes are effectively converted into vitamin A and generally are accepted to have much higher safety than vitamin A itself. Fruits and vegetables with high carotene content are not routinely available at affordable prices to poor people, and for those who can afford them appropriate food sources that are fortified with these precursors are not available. One of the most important contributions that biotechnology can make to world health is to produce crops naturally fortified with this important nutrient that people can grow in varied global regions and that would become part of their regular food intake. This also would reduce the need to exogenously fortify foods with nutrients produced outside of the plant. Fortification within the seed enhances nutritional quality for all types of farmers. With fortification, local crops grown by subsistence farmers and best suited to their growing conditions naturally would include these nutrients. Large, commercial farmers would reap the same benefit. This represents a whole new way of thinking about food fortification. Biotechnology could be used as a delivery system that benefits all levels of farming from the subsistence farmer to the large-scale, global grain grower. We have introduced the gene phytoene synthase into canola and demonstrated that the expression of this gene results in

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high levels of beta carotene accumulation within the rape seed (Table 1). Rape seed, popularly known as mustard seed, is grown in many parts of the world, including Africa, Asia, and Latin America, and its use is increasing. These are the same regions with high levels of vitamin A deficiency. Interestingly, in addition to containing high levels of beta carotene, rape seed oil expressing the phytoene synthase gene has a higher level of alpha carotene, lutein. In comparison with other sources of provitamin A, such as red palm oil, this annual crop has the ability to provide a varying range of carotenes, vitamin E, and a healthier profile of fatty acids. Harnessing the full genetic potential of the rape seed crop can go a long way toward addressing the nutritional needs of our evergrowing population—the high beta-carotene canola is expected to be commercialized within the next 3–4 years. While the example provided above illustrates the power of biotechnology for addressing the nutritional needs from the perspective of a well-established nutrient, the same technology can be harnessed to address the nutritional needs of even advanced countries of the world by producing new nutrients in grains. As our understanding of the human genome and the biochemical reactions associated with the onset of degenerative processes in the body increases, we are likely to understand the role of many nutrients in our food that can both accelerate as well as inhibit such processes. By using biotechnology, we can eliminate antinutrients (which will accelerate the degeneration of health and progression of disease) and increase the levels of nutrients that can help us live healthier lives. One example of such a nutrient is provided below. At the present time, cardiovascular diseases account for most deaths in Europe and North America and are becoming more prominent in urban societies in the rest of the world. The cost to society in the United States is estimated to be $260 billion annually from cardiovascularrelated disorders, including heart disease, coronary artery disease, stroke, hypertensive disease, and congestive heart failure. As described earlier, total and low density lipoprotein cholesterol are important biomarkers of cardiovascular health and are routinely monitored to assess the health status of individuals (15). High total cholesterol levels contribute to cardiovascular disease and levels below 200 mg/dl are desirable. Approximately 115 million people in the United States appear to have cholesterol levels between 200 and 239 mg/dl and have a higher risk of death caused by myocardial infarction (American Heart Association data). While people with cholesterol levels above 240 mg/dl are given prescribed drugs, drug therapy generally is not recommended for people with lower cholesterol levels in view of the considerations of cost, safety, etc. Very few people who have these intermediate levels of cholesterol strictly follow the recommended practice of reducing the saturated fat intake and exercising, thereby increasing the risk of contacting the disease and cost to society. It has been known for quite some time that phytosterols have the potential to reduce cholesterol in humans by 10–15% by interfering with cholesterol absorption in the gastrointestinal tract (16, 17). Indeed products containing these phytosterols such as Benecol and Take Control are beginning to appear in the market to assist individuals in managing their cholesterol levels more aggressively. Phytosterols are not currently available in adequate quantities in the foods that we ordinarily consume. It has been known for some time that expression of genes in the phytosterol pathway in plants increases the sterol content of plant tissues. Based on these and other novel genes, we now are working on increasing the phytosterol content of several grains.

Table 1. Composition of high carotenoid canola High carotenoid canola oil, µg/gm Carotenoids (Total) 2025–2466 β-carotene 690–920 α-carotene 470–530 Lycopene 8–33 Lutein 85–196 Phytoene 760–820 Tocopherols 400–500 400–500 Tocols

Red palm oil, µg/gm 480–672 280–392 175–245 7–9 0 10–15 90–150 600–1000

While the above example serves to illustrate the power of the technology in the context of cholesterol, several other nutrients and their relationship to human health now are being investigated. A range of fatty acids that modulate inflammatory reactions in the human body, and antioxidants that have sparing effects on antioxidant vitamins such as vitamin C and E and that also boost the levels of antioxidant defense enzymes in the human body are just a few examples of a multitude of discoveries that are likely to emerge in this area in the near future (18). Most of the progress to date has been made by using either single genes or first-generation molecular breeding capabilities. Rapid accumulation of sequence data from both chromosomal DNA and expressed sequence tags of plants and other species is giving us significant insights into the genetic makeup and functions of several genes in plants (19). Complementation of the sequence information with high throughput gene expression analysis and mutation/gain of function biological analysis is beginning to open the doors to a vista of knowledge on the role and functions of many of these genes. Plant genomics, which is only a few years old, is expected to provide whole new insights into designing crops that are superior in every aspect of both input and output traits that are described here. In summary, biotechnology adds value across the system from crop to farmer, customer and consumer. Biotechnology can, and is, enhancing the quality of food in addition to improving the quantity of food. Biotechnology can improve the sustainability of production systems by requiring fewer inputs to control pests and better protect the quality of water and land mass around us. Biotechnology can add health and vitality to humans. As we look at food production in a more holistic way, biotechnology will be an important component of that holistic system. We gratefully acknowledge the contributions of Diane Herndon and Tracy Farmer in preparing the manuscript. 1. Brown, L. R. (1998) State of the World: A Worldwatch Institute Report on Progress Toward a Sustainable Society (Norton , New York), p. 9 . 2. U.S. Bureau of Mines (1993) Minerals Today, 15 . 3. Brown, L. R. (1998) State of the World 1998: A Worldwatch Institute Report on Progress Toward a Sustainable Society (Norton, New York), p. 6 . 4. Hobbs, F. B. & Damon, B. L. (1996) 65+ in the United States (U.S. Government Printing Office , Washington, DC), U.S. Bureau of the Census, Current Population Reports, Special Studies , pp. 23–190 . 5. Kishore, G. & Shah, D. (1988) Annu. Rev. Biochem. 57, 627–663 . 6. Padgette, S. R. , Kolacz, K. H. , Delanny, X. , Re, D. B. , La Vallee, B. J. , Tinius, C. N. , Rhodes, W. K. , Otero, Y. I. , Barry, G. F. , Eichholtz, D. A. , et al. (1995) Crop Sci. 35, 1451–1461 . 7. Koziel, M. G. , Beland, G. L. , Bowman, C. , Carozzi, N. B. , Crenshaw, R. Crossland , L., Dawson, J. , Desai, N. , Hill, M. , Kadwell, S. , et al. (1993) Bio/Technology 12, 793–796 . 8. Perlak, F. J. , Ruchs, R. L. , Dean, D. A. , McPherson, S. L. & Fischhoff, D. A. (1991) Proc. Natl. Acad. Sci. USA 88, 3324–3328 . 9. Lichtenstein, A. H. , Ausman, L. M. , Carrusco, W. , Jenner, J. L. , Ordovas, J. M. & Schafer, E. J. (1993) Atheroscler. Thrombosis 123, 154–161 . 10. Kritchevsky, D. (1997) Prostaglandins Leukotrienes Essent. Fatty Acids 57, 399–402 . 11. Anonymous (1998) Int. News Fats Oils Relat. Mater. 9, 202–208 .

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12. WHO (1995) Global Prevalence of Vitamin A Deficiency (WHO , Geneva), Micronutrient Deficiency Information Systems Working Paper No. 2 . 13. Underwood, B. A. & Arthur, P. (1996) FASEB J. 10, 1040–1048 . 14. Somer, A. & West, K. P., Jr. , eds. (1996) in Vitamin A Deficiency: Health, Survival and Vision (Oxford Univ. Press, New York), pp. 19–98 . 15. Kritchevsky, D. (1995) Nutrition and Health, ed. Bronner, F.(CRC , Boca Raton, FL), pp. 89–112 . 16. Miettinen, T. A. , Puska, P. , Gylling, H. , Vanhannen, H. & Vartiainen, E. (1995) N. Engl. J. Med. 333, 1308–1312 . 17. Pedersen, T. R. (1995) N. Engl. J. Med. 333, 1350 . 18. Brower, V. (1998) Nat. Biotechnol. 16, 728–731 . 19. McCouch, S. (1998) Proc. Natl. Acad. Sci. USA 95, 1983–1985 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Use of plant roots for phytoremediation and molecular farming

DOLORESSA GLEBA * † , NIKOLAI V. BORISJUK † * , LUDMYLA G. BORISJUK * † , RALF KNEER * † , ALEXANDER POULEV * † , MARINA SKARZHINSKAYA , SLAVIK DUSHENKOV ‡ , SITHES LOGENDRA * , YURI Y. GLEBA § , AND ILYA RASKIN * ¶ ABSTRACT Alternative agriculture, which expands the uses of plants well beyond food and fiber, is beginning to change plant biology. Two plant-based biotechnologies were recently developed that take advantage of the ability of plant roots to absorb or secrete various substances. They are (i) phytoextraction, the use of plants to remove pollutants from the environment and (ii) rhizosecretion, a subset of molecular farming, designed to produce and secrete valuable natural products and recombinant proteins from roots. Here we discuss recent advances in these technologies and assess their potential in soil remediation, drug discovery, and molecular farming. Biotechnology is transforming world agriculture, adding new traits to crop plants at a greatly accelerated rate. Plants are becoming more efficient producers of food, fiber, medicines, and construction materials. In addition to these conventional uses, biotechnology opens doors to unique uses of plants that are gaining greater acceptance from the public and attention from the scientific community. These so-called “valueadded” uses include phytoremediation, the use of plants to remove pollutants from the environment or to render them harmless (1), and molecular farming (phytomanufacturing), the use of plants for the production of valuable organic molecules and recombinant proteins (2, 3). Because of the growing number of commercially successful applications and the lack of serious environmental concerns, both technologies are gaining acceptance from the scientific community, the general public, and regulators. With the exception of root crops, plant roots are less utilized and studied than shoots. However, this situation may be changing because of the emerging biotechnologies described below that exploit the ability of plants to transport valuable molecules into and out of their roots. These root-based technologies include metal phytoextraction, a subset of phytore-mediation, which uses plants to remove toxic heavy metals from soil; and rhizosecretion, a subset of molecular farming, which relies on the ability of plant roots to exude valuable compounds. Both technologies exploit plants’ innate biological mechanisms for human benefit. Phytoextraction. Giant underground networks formed by the roots of living plants function as solar-driven pumps that extract and concentrate essential elements and compounds from soil and water. Absorbed substances are used to support reproductive function and carbon fixation within shoots. Metal phytoextraction relies on metal-accumulating plants to transport and concentrate polluting metals, such as lead, uranium, and cadmium, from the soil into the harvestable aboveground shoots (1, 4, 5). Hydroponically grown plant roots can also directly absorb, precipitate, and concentrate toxic metals from polluted effluents in a process termed rhizofiltration (6). Chelate-assisted phytoextraction (1) has been successfully used to remove lead from contaminated soils using specially selected varieties of Indian mustard (Brassica juncea L.). These varieties combine high shoot biomass with the enhanced ability of roots to adsorb EDTA-chelated lead from soil solution and transport it into the shoots. The transpiration stream is likely to be the main carrier of soluble chelated metal to the shoots, where water is transpired while metal accumulates (5). Chelate-assisted phytoextraction was also successfully used to phytoextract uranium (7). One strategy for increasing the efficiency of phytoextraction is to increase metal translocation to the shoot by increasing plant transpiration. Earlier research showed that wind enhances metal flux to the shoots, while compounds that block transpiration (i.e., abscisic acid) block metal accumulation in the shoots (8). Spontaneous or chemically induced mutants with increased stomatal transpiration were isolated from various plant species, including tomato (9), Arabidopsis (10), and barley (11). To determine whether genetically increased transpiration would increase the efficiency of phytoextraction, (M1) seeds of B. juncea were mutagenized with ethyl methanesulfonate (EMS), and mature plants were self-pollinated to obtain M2 seeds. Ten- to fourteen-day-old M2 seedlings were screened by excising a middle leaf from each plant, laying it flat in a well-aerated room, and visually assessing the degree of tissue dehydration after 1 or 2 hours. Plants whose leaves wilted (lost water) faster than others were saved and rescreened later in hydroponics and in soil for increased transpiration to confirm the results of the initial screen. After screening 20,000 M2 seedlings, 47 plants with significantly increased leaf transpiration rates were identified. Line M-30, in which the transpiration rate exceeded that of the wild-type plants by 130% in soil and by 75% in hydroponics, was tested for its phytoextraction performance in lead-contaminated soil amended with 2.5 mmol of EDTA per kg of soil. This high-transpiration line phytoextracted 104% more lead than the wild-type B. juncea, making it a good candidate for field optimization and use. Increased resistance to metal is another important trait that can improve the efficiency of phytoextraction. Varieties of B. juncea with greater metal tolerance should grow better in metal-contaminated sites and survive longer after metal uptake is induced by chelate application to the soil. Substantial research has been directed toward isolating genes that are involved in metal biology, e.g., metallothioneins or transporters. Interestingly, some increases in cadmium tolerance were observed in transgenic plants overexpressing the human metallothioneinII gene (12). *

*

Biotech Center, Foran Hall, Cook College, Rutgers University, 59 Dudley Road, New Brunswick, NJ 08901-8520 ; D.G., N.V.B., L.G.B., R.K., A.P., and M.S. contributed equally to this work. ‡ Phytotech, Inc., 1 Deer Park Drive, Suite I, Monmouth Junction, NJ 08852 ; and § Institute of Cell Biology and Genetic Engineering, Zabolotnogo Street, 148, Kiev, DSP-22, 252650, Ukraine ¶ To whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org. †

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Valuable metal-resistance traits can be found in metal hyperaccumulating plants that are endemic to soils naturally enriched with heavy metals. These plants can accumulate exceedingly high amounts of essential and nonessential heavy metals in their foliage, to levels that are highly toxic to most other plants (13). For example, several Thlaspi species can accumulate Ni and Zn, to 1–5% of its dry biomass. This is an order of magnitude greater than concentrations of these metals in the nonaccumulating plants growing nearby. The prevention of herbivory and disease is thought to be the main function of this unique phenomenon (14, 15). It recently has been established that the ability of T. goesingense Halacsy to hyperaccumulate metals is the result of high resistance to the metals rather than the greater rates of metal uptake (16). Unfortunately, most hyperaccumulating species are not suitable for phytoextraction for several reasons: (i) metals that are primarily accumulated (Ni, Zn, and Cu) are not among the most important environmental pollutants; (ii) most have very low biomass and capricious growth habits unsuitable for monoculture; and (iii) agronomic practices and crop protection measures for their cultivation have not been developed. However, many metalhyperaccumulating species belong to Brassicaceae (mustard) family, and thus are related to B. juncea, the preferred plant for phytoextraction of lead. Unfortunately, B. juncea, while exhibiting a high capacity for metal uptake and translocation, is not very resistant to high levels of lead or other heavy metals in its foliage. Therefore, chelate-assisted phytoextraction is very toxic to B. juncea, requiring harvesting several days after chelate application. Unfortunately, no genes conferring metal resistance were identified in any of the hyperaccumulating species, precluding the possibility of direct gene transfer. Thus, an attempt was made to introduce metal resistant traits into the high-biomass Pb accumulator B. juncea using somatic hybridization. Thlaspi caerulescens, a known Ni and Zn hyperaccumulator, was selected as one of the parents for both symmetric and asymmetric hybrids in which T. caerulescens protoplasts were irradiated with x rays before fusion. Eighteen hybrids were regenerated, all showing a phenotype intermediate between those of the parents. Two asymmetric hybrids were found to be fertile. One of these hybrids (60/31) had vigorous growth, characteristic of B. juncea, and contained Thlaspi-specific repetitive DNA sequences, as demonstrated by Southern hybridization. (As expected, total DNA from B. juncea parent did not hybridize with Thlaspi-specific probes). Hybrid 60/31 displayed dramatically increased resistance when germinated and grown in Pb-, Ni-, and Zn-contaminated soil (Fig. 1). The amount of Pb that the hybrid was able to phytoextract on a dry weight basis was similar to that of both parents. However, the total amount of Pb phytoextracted by each hybrid plant was much greater because of the greater biomass produced on the contaminated soil. Interestingly, the growth habits and biomass of B. juncea and the 60/31 hybrid did not differ much when the plants were grown in noncontaminated fertile soil (data not shown).

FIG. 1. Asymmetric somatic hybrid 60/31 (B) and its parents Brassica juncea (A) and Thlaspi caerulescens (C) growing in soil containing 800 mg/kg lead, 328 mg/kg nickel, and 7,600 mg/kg zinc. Rhizosecretion. Phytoextraction exploits the ability of plant roots to remove unwanted contaminants from their environment. But could the reverse of this process also be exploited? Could roots make valuable compounds and deliver them into their environment? At present, most of the recombinant proteins or valuable natural products used as fine chemicals, pharmaceuticals, crop protection compounds, cosmetic ingredients, etc. are extracted from plants by using solvents. This method requires expensive purification of the active ingredients from complex mixtures of organic molecules and proteins, making downstream processing and purification of individual components difficult and costly. Extracting plants is also a “batch” process whereby the plant is harvested, and its continual ability to synthesize chemicals is not utilized. Natural rubber and maple syrup are rare examples of continuous manufacturing processes, which produce much larger amounts of valuable plant product over the lifetime of the plant. Rhizosecretion of Natural Products. In addition to accumulating biologically active chemicals, plant roots continuously produce and secrete compounds into their immediate environment (rhizosphere). While up to 10% of photosynthetically fixed carbon is secreted from the roots (17, 18), the systematic study of chemical composition of root exudates from diverse plant species has not been undertaken. Not surprisingly, few compounds that were identified in root exudates were shown to play an important role in several biological processes. For example, isoflavonoids and flavonoids present in the root exudates of a variety of legume plants activate the Rhizobium genes responsible for the nodulation process (19, 20) and, possibly, for vesicular–arbuscular mycorrhiza (VAM) colonization (21). Strigol, a germination stimulant for the parasitic plant Striga asiatica, has been found in the root exudates of many cereals (22). A variety of plants produce herbicidal allelochemicals that may inhibit growth and germination of neighboring plants (23–25). In addition, root-secreted compounds called phytosiderophores may be involved in the acquisition of essential plant nutrients from soils (26–28) and in defense against toxic metals such as aluminum (29). Intuition and limited published data (30) suggest that root-secreted compounds should have a wide spectrum of biological activities including protection against biotic and abiotic stresses. Survival of delicate and physically unprotected root cells may depend on their continuous “underground chemical warfare” against a hostile and constantly changing environment teeming with bacteria and fungi preying on any organic material in soil. The unexplored chemical diversity of root exudates is an obvious place to search for novel biologically active compounds including antimicrobials. Our biochemical analysis of root exudates from 120 plant species can be summarized as follows: (i) each plant species studied exuded a distinct set of compounds, which is a unique biochemical fingerprint for a given species (Fig. 2 A–C); (ii) root exudates are relatively simple mixtures, in comparison to solvent extracts of plant tissue, making the isolation of the active molecules an easier task; (iii) root exudates are devoid of pigments and tannins, known to interfere in activity screens, and do not contain large quantities of biologically inert structural compounds; and (iv) the chemical composition of root exudates is very different from that of conventional methanolic extracts of root tissue. We have also observed that exudate chemical diversity can be greatly increased by the elicitation process, which is known to alter secondary metabolism in plants exposed to various physical and chemical treatments. Phytoalexins, antimicrobial compounds produced in plants and tissue cultures in response to disease causing agents or their chemical components, are

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probably the best studied elicited defense compounds in plants (31). Unfortunately, little is known about elicited compounds in root exudates, with the exception of a recent report on isoflavonoid exudation from the roots of white lupine (30). We observed that chemical or physical elicitors stimulate roots of various plants to exude an array of compounds not detected in the “nonelicited” exudates (Fig. 2 D–F). On the other hand, the same elicitor will trigger the production of different compounds in different plant species. In addition, elicitation may dramatically increase the quantities of certain compounds in the exudates. It can be hypothesized that elicitors mimic the effects of stresses on the hydroponically grown roots, activating biochemical defense systems and resulting in quantitative and qualitative changes in the composition of the exudates.

FIG. 2. HPLC profiles of nonelicited root exudates of three plant species collected in distilled water (A–C) and root exudates of Brassica juncea collected in distilled water (D) or in distilled water supplemented with 1 mM AgNO3 (E) or 500 mM H2O2 (F) as elicitors. Plants were grown hydroponically with roots suspended in aerated nutrient solution. Root exudates from 4- to 6-week-old plants were collected for 24 hours in 400 ml of distilled water with or without elicitors. Root exudates were concentrated by freeze-drying, and exudate compounds were separated on a Waters NovaPak C-18 reverse phase column using acetic acid/acetonitrile gradient. To demonstrate the presence of antimicrobial compounds in root exudates, a screening protocol was designed in which 10 µl of concentrated exudate solution was transferred into a small cavity in agar poured into 24-well microtiter plates. The tested microorganisms were plated in each well before the cavity was made. Exudates from 480 species, each treated with 2–4 elicitors, were tested in this system for the inhibition of growth of selected bacteria and fungi (Fig. 3). The following percentage of exudates showed moderate to strong activity against tested microorganisms: Escherichia coli (3.4%), Staphylococcus aureus (4.3%), Pseudomonas aeruginosa (0.4%), Penicillium notatum (0.8%), and Saccharomyces cerevisiae (0.6%). In addition to exudates, hydroponically cultivated plant roots also provide a unique source of biologically active compounds. We have also observed that elicitation, both quantitatively and qualitatively, alters the HPLC profiles of secondary metabolites in roots of many plant species (data not shown). Most likely, these changes are subsequently reflected by the dramatic alterations in the rhizosecreted compounds. Why Root Exudates? The above observations suggest that root exudates represent a new and functionally enriched source of biologically active compounds. Elicitation of hydroponically grown roots adds another unexplored dimension to the chemical diversity normally hidden in silent parts of the plant genomes. In addition to shedding light on dark corners of plant biology, the systematic study of root exudates may be valuable to the global pharmaceutical industry, which still heavily relies on novel sources of chemical diversity to discover new drugs in an ever-accelerating race against time. Twenty five percent of all prescriptions dispensed from pharmacies in the United States contain active ingredients extracted from higher plants (32). However, methods of harvesting chemical diversity of plant-derived compounds often follows hunter–gatherer strategies. Extracts of plant material haphazardly collected in various places around the world are eventually acquired by pharmaceutical companies, which put them through sophisticated high-throughput screens that use an increasing array of molecular targets. This primitive prospecting process does not provide a reliable and reproducible source of natural products that can be easily resupplied after a novel activity is found. The mismatch between the beginning of the drug development pipeline and what follows creates an opportunity for developing new pharmaceutical agents from plants using more standardized, scientific approaches that favor biologically active

FIG. 3. Antimicrobial activity of root exudates. The exudates showing activity (indicated with red arrows) against Staphylococcus aureus ssp. aureus (A) were from Tagetes minuta (column 1, Asteraceae) and Eriastrum densiflorum var. austromontana (column 6, Polemoniaceae) and activity against Saccharomyces cerevisiae (B) were from Hosta fortunea (column 6, Liliaceae). To test antibacterial/ antifungal activity of exudates, the suspension of target microorganisms or spores was plated and spread on the surface of standard LB agar (bacteria) or potato dextrose agar (fungi) poured into 24-well microplates. Twenty microliters of exudate dissolved in water was pipeted into a central hole punched in the agar. The antimicrobial activity, visible as an area of growth inhibition (clearing) around the central hole was scored after 24 hours of incubating inoculated plates at 30°C.

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molecules over structural components and major metabolites. Tissue culture-based production of natural products, often combined with elicitation, is one of the recently developed strategies for “increasing the size of the needle in the haystack.” However, plant tissue cultures are expensive, slow growing, and relatively deficient of secondary metabolites, presumably because of their nondifferentiated nature. Rhizosecretion, on the other hand, may produce a more cost-effective and diverse source of chemical compound mixtures for the identification of novel biologically active compounds. In addition, rhizosecretion, a nondestructive and continuous process, may provide a constant supply of these compounds over the lifetime of a plant.

FIG. 4. Rhizosecretion of jellyfish green fluorescent protein (GFP)(A), human placental alkaline phosphatase (SEAP)(B), and bacterial (Clostridium thermocellum) xylanase (C) from the roots of transgenic Nicotiana tabacum L. (A) To direct GFP into the secretory pathway, GFP-coding sequence was fused to the signal peptide derived from the resident ER protein calreticulin, and the resulting fusion placed in correct orientation between the mannopine synthase (mas2
) promoter (provided by Stanton Gelvin, Purdue University, West Lafayette, IN) and nos terminator. GFP rhizosecretion from the hydroponically cultivated aseptic roots was visualized after illuminating the hydroponic medium contacting roots with nearUV light. Media from nontransformed plants showed no fluorescence (data not shown). (B) Visualization of SEAP rhizosecretion in the native gel. In transformed tobacco, coding sequence of SEAP with its own signal peptide was controlled by the cauliflower mosaic virus 35S promoter (CaMV35S). Thirty micrograms of total protein concentrated from root exudates of transgenic and nontransformed plants was separated on native PAGE, and SEAP activity was localized using the alkaline phosphatase isoenzymes procedure (Sigma). Lanes 1 and 2, transgenic tobacco plants; lanes 3 and 4, nontransformed tobacco. (C) Rhizosecretion of bacterial xylanase from transgenic tobacco seedlings germinated on the RBB-xylanecontaining agar medium (dark blue), which becomes colorless when cleaved by xylanase (photographed upside down). Nontransformed plants did not change the color of the medium (data not shown). Seeds of tobacco expressing a truncated C. thermocellum xylanase gene controlled by the CaMV35S promoter and targeted to the apoplast by proteinase inhibitor II ER signal peptide were provided by Uwe Sonnewald. Rhizosecretion of Recombinant Proteins. The ease of transformation and cultivation make plants suitable for manufacturing many recombinant proteins. Indeed, numerous heterologous (recombinant) proteins have been produced in plant leaves, fruits, roots, tubers, and seeds (33–35), and are targeted to different subcellular compartments, such as the cytoplasm, endoplasmic reticulum (ER), or apoplastic space (36). Plants are capable of carrying out acetylation, phosphorylation, and glycosylation as well as other posttranslational protein modifications required for the biological activity of many eukaryotic proteins. However, the extraction and purification of proteins from biochemically complex plant tissues is a laborious and expensive process that presents a major obstacle to large-scale protein manufacturing in plants. In attempts to overcome this problem, secretion-based systems utilizing transgenic plant cells or plant organs aseptically cultivated in vitro have been investigated (37–39). However, these in vitro systems, which include hairy roots, may be expensive, slow-growing, unstable, and relatively low-yielding. Until now, these disadvantages precluded the use of in vitro plant systems for the commercial manufacturing of recombinant proteins. Can rhizosecretion be used for the continuous manufacturing of recombinant proteins? The nondestructive rhizosecretion process may provide high yields of recombinant proteins over the lifetime of a plant and facilitate their downstream purification, combining the advantages of the whole plant and in vitro protein expression systems. Indeed, roots of living plants are known to secrete proteins. For example, large amounts of acid phosphatase are released from the roots of many plants during phosphate deficiency (40). We attempted to “rhizosecrete” the following three heterologous proteins of different origins from Nicotiana tabacum L.; green fluorescent protein (GFP) of the jellyfish Aequorea victoria, human placental secreted alkaline phosphatase (SEAP), and xylanase from the thermophylic bacterium Clostridium thermocellum. All three of these proteins were rhizosecreted from transgenic plants when their expression was controlled by a strong root-expressed promoter and targeted by a secretory signal peptide (Fig. 4). Daily rhizosecretion of GFP, released into fresh medium unprotected from proteolysis, reached 2 µg/g root dry weight, while SEAP rhizosecretion, quantified from its activity, reached 20 µg/g root dry weight, a significant amount considering that no attempts to optimize rhizosecretion had been made thus far. It is likely that methods for increasing protein expression and secretion will be developed along with plant varieties optimized for the rhizosecretion of recombinant proteins. Data suggest that plant roots can continuously produce and secrete biologically active recombinant proteins of different origins. The rhizosecretion system offers a simplified method for the isolation of recombinant proteins from simple hydroponic medium rather than from complex plant extracts. As with rhizosecretion of natural products, protein rhizosecretion can be operated continuously without destroying the plant, thus producing a higher total yield of the recombinant protein over the life of the transgenic plant. In addition, recombinant biopharmaceutical proteins purified from root exudates are less likely to be contaminated with pathogenic viruses that may be present in the milk or urine of transgenic animals. Rhizosecretion also borrows from many well developed and tested methods of commercial hydroponic plant cultivation, and therefore, will be relatively easy to scale up.

CONCLUSIONS While the evolution of plant shoots followed primarily “introverted” paths by perfecting physical barriers between themselves and the environment, roots had to be more “extroverted” in their relationship with soil. This requirement created a unique set of biological mechanisms, which until recently, were understudied and underutilized. Phytoextraction and rhizosecretion are starting to change this, while allowing scientists to take a radically new look at the darkest corners of plant biology. These technologies also open the doors to the value-added, nonagricultural uses of plants, which will continue to expand in the new century.

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Neither phytoextraction nor rhizosecretion will directly contribute to feeding world population in the next century. However, these technologies will improve the quality of life for many people if their development continues. The future challenge for metal phytoextraction is to further reduce the cost and increase the spectrum of metals amenable to this technology. This goal can be achieved by creating superior plant varieties for phytoextraction by using genetic engineering to introduce valuable traits into plants, developing better agronomic protocols for their cultivation, and designing safer and more effective soil amendments. A recent, and probably the only, example of the successful use of genetic engineering applied to metal phytoremediation is the use of bacterial mercuric reductase (merA) gene to achieve mercuric ion reduction in transgenic Arabidopsis (41) and yellow poplar plants (42). Elemental mercury produced in transgenic plants is much less toxic than ionic mercury and can be volatilized from transgenic plants in a process termed phytovolatilization, which is related to phytoextraction. The future challenge for rhizosecretion lies in the successful development of effective and safe pharmaceuticals from the collection of biologically active lead molecules secreted by the roots, and in large-scale, cost-effective manufacturing of recombinant proteins. The aging population and ever-growing demand for better pharmaceuticals should foster the use green plants as sources of new drug discovery, biotransformation, and in some cases, manufacturing. Thus, more effective utilization of immense biosynthetic capacity of plants based on their inexpensive and renewable nature will present major opportunities for plant researchers in the next century. 1. Salt, D. E. , Smith, R. D. & Raskin, I. (1998) Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 643–668 . 2. Nawrath, C. , Poirier, Y. & Somerville, C. (1995) Mol. Breeding 1, 105–122 . 3. Franken, E. , Teuschel, U. & Hain, R. (1997) Curr. Opin. Biotechnol. 8, 411–416 . 4. Kumar, P. B. A. N. , Dushenkov, V. , Motto, H. & Raskin, I. (1995) Environ. Sci. Technol. 29, 1232–1238 . 5. Vassil, A. D. , Kapulnik, Y. , Raskin, I. & Salt, D. E. (1998) Plant. Physiol. 117, 447–453 . 6. Dushenkov, V. , Kumar, P. B. A. N. , Motto, H. & Raskin, I. (1995) Env. Sci. Technol. 29, 1239–1245 . 7. Huang, J. W. , Blaylock, M. J. , Kapulnik, Y. & Ensley, B. D. (1998) Environ. Sci. Technol. 32, 2004–2008 . 8. Salt, D. E. , Prince, R. C. Pickering, I. J. & Raskin, I. (1995) Plant Physiol. 109, 1427–1433 . 9. Tal, M. (1966) Plant Physiol. 41, 1387–1391 . 10. Koornneef, M. , Reuling, G. & Karssen, C. M. (1984) Physiol. Plant. 61, 377–383 . 11. Raskin, I. & Ladyman, J. A. R. (1988) Planta 173, 73–78 . 12. Misra, S. & Gedamu, L. (1989) Theor. Appl. Genet. 78, 161–168 . 13. Baker, A. J. M. & Brooks, R. R. (1989) Biorecovery 1, 81–126 . 14. Boyd, R. S. & Martens, S. N. (1994) Oikos 70, 21–25 . 15. Boyd, R. S. , Shaw J. J. & Martens, S. N. (1994) Am. J. Bot. 81, 294–300 . 16. Kramer, U. , Smith, R. D. , Wenzel, W. W. , Raskin, I. & Salt, D. E. (1997) Plant Physiol. 115, 1641–1650 . 17. Johansson, G. (1992) Soil Biol. Biochem. 24, 427–433 . 18. Shepherd, T. & Davies, H. V. (1993) Ann. Bot. 72, 155–163 . 19. Peters, N. K. & Long, S. R. (1988) Plant Physiol. 88, 396–400 . 20. Maxwell, C. A. & Phillips, D. A. (1990) Plant Physiol. 93, 1552–1558 . 21. Tsai, S. M. & Phillips, D. A. (1991) Appl. Environ. Microbiol. 57, 1485–1488 . 22. Siame, B. A. , Weerasuriya, Y. , Wood, K. , Ejeta, G. & Butler, L. G. J. (1993) Agric. Food Chem. 41, 1486–1491 . 23. Friebe, A. , Schulz, M. , Kuck, P. & Schnabel, H. (1995) Phyto-chemistry 38, 1157–1159 . 24. Yu, J. Q. & Matsui, Y. J. (1994) Chem. Ecol. 20, 21–31 . 25. Inoue, M. , Nishimura, H. , Li, H. H. & Mizutani, J. (1992) J. Chem. Ecol. 18, 1833–1840 . 26. Miyasaka, S. C. , Buta, J. G. , Howell, R. K. & Foy, C. D. (1991) Plant Physiol. 96, 737–743 . 27. Lipton, D. S. Blanchar, R. W. & Blevins, D. G. (1987) Plant Physiol. 85, 315–317 . 28. Mori, S. , Nishizawa, N. , Kawai, S. , Sato, Y. & Takagi, S. J. (1987) Plant Nutr. 10, 1003–1011 . 29. de la Fuente, J. B. M. , Ramirez-Rodriguez, V. , Cabrera-Ponce, J. B. L. & Herrera- Estrella, L. (1997) Science 276, 1566–1568 . 30. Gagnon, H. & Ibrahim, R. K. (1997) Phytochemistry 44, 1463–1467 . 31. Dixon, R. A. (1986) Biol. Rev. 61, 239–291 . 32. Farnsworth, N. R. & Morris, R W. (1976) Am. J. Pharm. 148, 46–52 . 33. McGarvey, P. B. , Hammond, J. , Dienelt, M. M. , Hooper, D. C. , Fu, Z. F. , Dietzschold, B. , Koprowski, H. & Michaels, F. H. (1995) Bio/ Technology 1484–1487 . 34. Van Engelen, F. A. , Schouten, A. , Molthoff, J. W. , Roosien, J. , Salinas, J. , Dirkse, W. G. , Schots, A. , Bakker, J. , Gommers, F. J. , Jongsma, M. A. , et al. (1994) Plant Mol. Biol. 26, 1701–1710 . 35. Sonnewald, U. , Hajirezaei, M-R. , Kossmann, J. , Heyer, A. , Trethewey, R. N. & Willmitzer, L. (1997) Nat. Biotechnol. 15, 794–797 . 36. Conrad, U. & Fiedler, U. (1998) Plant. Mol. Biol. 38, 101–109 . 37. Li, J. , Hegeman, E. , Hanlon, R. W. , Lacy, G. H. , Cenbow, D. M. & Grabau, E. A. (1997) Plant Physiol. 114, 1103–1111 . 38. Firek, S. , Draper, J. , Owen, M. R. L. , Gandecha, A. , Cockburn, B. & Whitelam, G. C. (1993) Plant Mol. Biol. 23, 861–870 . 39. Wongsamuth, R. & Doran, P. M. (1997) Botechnol. Bioeng. 54, 401–415 . 40. Li, M. & Tadano, T. (1996) Soil Sci. Plant Nutr. 42, 753–763 . 41. Rugh, C. L. , Wilde, H. D. , Stack, N. M. , Thompson, D. M. , Summers, A. O. & Meagher, R. B. (1996) Proc. Natl. Acad. Sci. USA 93, 3182–3187 . 42. Rugh, C. L , Senecoff, J. F. , Meagher, R. B. & Merkle, S. A. (1998) Nat. Biotechnol. 16, 925–928 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Transgenic plants for tropical regions: Some considerations about their development and their transfer to the small farmer

LUIS HERRERA ESTRELLA * Departamento de Ingeniería Genética, Centro de Investigación y Estudios Avanzados, Apartado Postal 629 C.P. 36500 Irapuato, Guanajuato, Mexico ABSTRACT Biotechnological applications, especially transgenic plants, probably hold the most promise in augmenting agricultural production in the first decades of the next millennium. However, the application of these technologies to the agriculture of tropical regions where the largest areas of low productivity are located, and where they are most needed, remains a major challenge. In this paper, some of the important issues that need to be considered to ensure that plant biotechnology is effectively transferred to the developing world are discussed. The world’s population is expected to double by the year 2050, making food security the major challenge for the next millennium. Food production will have to be doubled or preferably tripled by the year 2050 to meet the needs of the expected 11 billion people, of whom ninety percent will reside in the developing world. The enormity of the challenge is significantly increased by the declining availability of water and the fact that this additional food will have to be produced on existing agricultural land or in regions considered as marginal soils, if we want to preserve the forested regions and the environment as a whole. Agricultural research and technological improvements are, and will continue to be, required for increasing agricultural productivity. There are numerous ways in which agricultural productivity may be increased in a sustainable way, including the use of biological fertilizers, improved pest control, soil and water conservation, and the use of improved plant varieties, produced by either traditional or biotechnological means. Of these measures, biotechnological applications, especially transgenic plant varieties, probably hold the most promise for augmenting agricultural production and productivity, when properly integrated into traditional systems. The Case for Genetically Engineered Plants. The effectiveness of transgenic plant varieties in increasing production and lowering production cost has been demonstrated in the cases of virus-, insect-, and herbicide-resistant plants, in which an average increase in production of 5% to 10%, and a saving in herbicides of up to 40% and in insecticides of between $60 to $120 per acre, have been reported in 1996 and 1997 (1). However, these increases in productivity, impressive as they are in terms of their economic and environmental value, will have a limited impact for global food supply. In fact, most of the developments in transgenic crops are aimed either at reducing production costs in agricultural areas that already have high productivity levels or at increasing the value added to the final product by improving, for instance, oil quality. This trend has been stimulated by the current policies of developed countries to limit production of key products such as cereals, meat, and dairy products because of the reductions in international prices of these products, and to reduce the intensive use of fertilizers and pesticides because of their deleterious effects on the environment. In a global sense, a more effective strategy would be to increase productivity in tropical areas, where an increase in food production is needed and where crop yields are significantly lower than those obtained in developed countries. In tropical areas, the losses caused by pests, diseases, and soil problems are exacerbated by climatic conditions that favor high levels of insect pests and vectors and by the lack of the economic resources to apply insecticides and fertilizers and to purchase high-quality seeds. In addition to low productivity levels, postharvest losses in tropical areas are very high, again because of climatic conditions that favor fungal and insect infestation and because of the lack of appropriate storage facilities. Despite efforts to prevent preharvest and postharvest crop losses, pests destroy over half of all world production. Preharvest losses caused by insects, the majority of which occur in the developing world, are calculated at around 15% of the world’s production. Using biotechnology to produce transgenic plants that better withstand diseases, insect attack, or unfavorable soil conditions, is not a simple task. There are an estimated 67,000 species of insects worldwide that damage crops and a similar or even higher number of plant pathogens. For instance, in the case of Phaseolus vulgaris, over 200 diseases and 200–300 species of insects can affect bean productivity (2). These numbers give an idea of the complexity of the task that scientists face in increasing productivity. There are of course a certain number of diseases and insect pests that can be singled out as the most important constraints for the production of each crop. However, it is also true that when a particular disease or insect pest is controlled, others considered as minor can then flourish, and themselves become major productivity constraints. One of the major advantages of plant biotechnology is that it can generate strategies for crop improvement that can be applied to many different crops. In this sense, genetically engineered virus resistance, insect resistance, and delayed ripening are good examples of strategies that can benefit many different crops. Transgenic plants of over 20 plant species that are resistant to more than 30 different viral diseases have been produced by using different variations of the pathogen-derived resistance strategy. Insect-resistant plant varieties, using the δ-endotoxin of Bacillus thuringiensis, have been produced for several important plant species including tobacco, tomato, potato, cotton, walnut, maize, sugarcane, and rice. Of these, maize, potato, and cotton are already under commercial production. It is envisaged that these strategies can be used for many other crops important for developing countries. Genetically engineered delayed ripening, although tested only on a commercial scale for tomato, has an enormous potential application for tropical fruit crops, which suffer severe losses because they ripen rapidly, and in many developing countries there are neither appropriate storage conditions nor adequate transportation systems to allow their efficient commercialization.

*To

whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org.

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To date, most of the developments in plant gene transfer technology and the different strategies for producing improved transgenic plant varieties have been driven by the economic value of the species or the trait. These economic values are in turn mainly determined by their importance to agriculture in the developed world, particularly the United States and Western Europe. This economical emphasis is understandable, because important investments are needed to develop, field test, and commercialize new transgenic plant varieties. However, in terms of global food production, it is necessary to ensure that this technology is effectively transferred to the developing world and adapted to the local crops and/or local varieties of crops for which it was originally developed. Developing improved transgenic versions of local varieties or local crops is not a trivial issue; in most, if not all, cultures, the use of specific crops has a deep social and/or religious meaning. Cultural preservation is just as important as environmental preservation. Cultural aspects of technology transfer need to be considered because simply replacing crops to increase productivity could have an enormously negative effect for certain cultures, and new introductions may not be accepted easily for human consumption. It is unfortunate that most developing countries do not have sufficient resources to implement the biotechnological capacity needed to solve the major problems that limit agricultural productivity, at least not in the time frame that is required to cope with the increasing demand for food. However, it is in the developing world that biotechnology could have its major impact in increasing crop production, especially in the areas of the world where yields are low because of the lack of technology. Plant genetic engineering could be considered a neutral technology that in principle does not require major changes in the agricultural practices of farmers in developing countries. Perhaps more importantly, it has the potential to bring about great benefits to the small farmers who lack the economic resources to purchase agrochemicals or prevent postharvest losses because of the lack of storage facilities. Whether there is time to increase agricultural productivity in the developing world is a question with a complex answer, because there are many factors that need to be taken into account to make this happen. We need to identify and establish mechanisms of technology transfer from developed countries, from both academic institutions and the private sector, to the developing world; there is a need to create a sufficient number of research centers with the capability of acquiring this technology, adapting it to local crops, and developing their own technologies. Seed production facilities must be improved and an effective mechanism implemented to reach subsistence farmers with this new technology. To meet these requirements, several economic, political, and social issues must be dealt with to ensure the general application of plant biotechnology to the agriculture of developing countries. The discussion of these issues goes beyond the scope of this article. However, it is my personal opinion that it will not be technological limitations but rather political and/or economic constraints that will determine how successful we are in supplying food to the hundreds of millions of people who will be malnourished in the next millennium. Soil Acidity: A Problem for Agriculture in the Tropics. Estimates of the world’s potentially arable land resources indicate that only 10.6% of the total land area of the world is cultivated, and about 24.2% is considered cultivable or is potentially arable land (3–5). Of these 2.5 billion hectares of potentially cultivable land, 68% is located in the humid tropics (6). The acid soils of the tropics, especially in the savannas, that historically have resisted permanent settlement and agricultural use are considered to represent the largest remaining potential for future agricultural development (7). There are problems limiting food production that are specific or more significant to the agriculture of tropical and subtropical regions, but that unfortunately have not been given sufficient importance to deserve being considered priorities in the research being done in developed countries. However, solutions to these problems could significantly contribute to food production in tropical areas. Because many of these problems are common to many developing countries and affect the productivity of a wide spectrum of crops, transgenic strategies to solve them that can be applied to different plant species are urgently needed. Among the problems common to tropical regions, probably the most important is soil acidity. On a global scale, there are two main geographical belts of acid soils: the humid northern temperate zone that is covered by coniferous forest and the humid tropics, which are (or in some cases were) covered mainly by savanna and tropical rain forest. Soil acidification can develop naturally in humid climates when basic cations are leached from soils but can be considerably accelerated by certain farming practices and by acid rain (8). Acidic soils comprise about 3.95 billion hectares of the ice-free land or approximately 40% of the world’s arable land. Regions with subsoil acidity occupy about 20% of the ice-free land surface. Approximately 43% of the world’s tropical land area is classified as acidic, comprising about 68% of tropical America, 38% of tropical Asia, and 27% of tropical Africa (9, 6). Tropical Acid Soils That Could Be Used for Agriculture. Because a great proportion of forest land is located in acid soils, it is important to remember that not all soils, although potentially arable land, can be used for agriculture. Tropical forests are invaluable with regard to their role in local, regional, and global ecosystems and to the biodiversity found within them (over 90% of plant and animal species live in forest ecosystems). Indiscriminate conversion of tropical forest into agricultural land will have far-reaching ecological consequences, whose effects will certainly outweigh the potential gain in food production. In spite of these consequences, 11 million or so hectares of forest are cleared every year, of which only a small fraction is converted into productive agricultural land, and most of it becomes unproductive grassland (6). Policies to use acid soils for agriculture should be directed to the acid savannas of the world such as the Cerrado in Brazil, Los Llanos of Venezuela and Colombia, the savannas in Africa, and the largely anthropic savannas of tropical Asia. These acid savannas cover an area of over 700 million hectares (which is approximately 50% of the global area that is currently under cultivation), and their potential in food production for both humans and animals could account for a large portion of that required to satisfy the need of the growing population in the next millennium. There are good examples in Brazil and Asia of successful development of acid savanna into productive land for the cultivation of sugarcane and soybean (6). The use of biotechnology could facilitate enormously the conversion of low-productivity acid savannas into productive cropland. Aluminum Toxicity. Poor crop productivity and soil fertility in acid soils are mainly caused by a combination of aluminum and manganese toxicity and nutrient deficiencies (mainly deficiencies in P, Ca, Mg, and K). Among these problems, aluminum toxicity has been identified as the most important constraint for crop production in acid soils. Aluminum toxicity problems are of enormous importance for the production of maize, sorghum, and rice in developing countries located in tropical areas of Asia, Africa, and Latin America. Most maize, sorghum, and rice cultivars currently being used are susceptible to toxic aluminum in the soil, and decreases in yield of up to 80% resulting from aluminum toxicity have been extensively reported in the literature (10–12). In particular, maize and sorghum production is severely limited in tropical Africa, where over 45% of the total land area in countries such as Zaire, Zambia, and the Ivory Coast is covered by acidic soils. In tropical South America, aluminum toxicity is a problem shared by several countries, where about 850 million hectares, or 66% of the region, has acid soils. In Brazil alone, acid savannas with low cation exchange capacity and high toxic aluminum

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saturation cover 205 million hectares, of which 112 million are suitable for maize and sorghum production (9). Aluminum has a clear toxic effect on roots, disturbing plant metabolism by decreasing mineral nutrition and water absorption. The most easily recognized symptom of Al toxicity is the inhibition of root growth, and this has become a widely accepted measure of Al stress in plants. Although Al toxicity primarily restricts root growth, given sufficient exposure, myriad different symptoms appear on both roots and shoots that are often mistaken for soil nutrient deficiencies. Therefore, crop production in acid soils is, to a great extent, limited by nutrient uptake deficiency caused by the inhibition of root growth and function that results from the toxic effects of Al (13). Moreover, in some acid soils, plant growth is affected not only by aluminum toxicity but also by low availability of some essential elements such as P, Ca, Mg, and Fe, some of which form complexes with Al and consequently are not readily available for root uptake (14). It is well documented that many plant species exhibit significant genetic variability in their ability to tolerate Al. Although it is clear that certain plant genotypes have evolved mechanisms that confer Al resistance, the cellular and molecular basis for Al resistance is still poorly understood (13). Two basic strategies by which plants can tolerate Al have been proposed: (i) the ability to exclude Al entry into the root apex and root hairs, and (ii) the development of mechanisms that allow the plant to tolerate toxic concentrations of Al within the cell. Several conceptually attractive hypotheses have been proposed to explain how plants could exclude Al from entering into the root. For example, mechanisms based on alteration in rhizosphere pH, low cell-wall cation-exchange capacity, or Al +3 efflux across the plasma membrane (13). However, experimental evidence from several research groups supports a mechanism that results in Al exclusion from the root apex via the release of Al-binding ligands such as malic and citric acids. When these ligands are released into the rhizosphere, they can effectively chelate Al+3 and prevent its entry into the root. The potential role of organic acid release in Al tolerance was originally proposed by Miyasaka et al. (15). Their work showed that the root system of an Al-tolerant snapbean cultivar grown in Al-containing solutions released 10 times as much citrate as an Al-sensitive cultivar grown in the presence of Al. The most complete analysis of the possible role of organic acids as Al+3-chelating molecules in naturally resistant plants comes from the work, done by Delhaize and coworkers (16, 17), using near-isogenic wheat lines differing at the Al tolerance locus (Alt1). These researchers found that, on treatment with Al, tolerant wheat varieties release 5- to 10-fold more malate than do susceptible lines, and that this increased capacity to excrete malate correlated with Al resistance and Al exclusion from the root apex. Because malic acid excretion is located in the root apex, the amount of malic acid excreted depended on the external Al concentration, and the Al tolerance cosegregates with high rates of malate excretion, Delhaize et al. (16, 17) proposed that the Alt1 locus in wheat encodes a component of an Al-tolerance mechanism based on the Al-stimulated excretion of malic acid. The existence of Al-tolerance mechanisms based on the excretion of organic acids has also been reported for plant species other than wheat: citrate in the case of maize, snap beans, and Cassia tora (18–20), and oxalic acid for buckwheat (Fagopyrum esculentum Moench) (20). An Example of How Transgenic Plants Could Improve Productivity in Acid Soils. The production of Al-tolerant transgenic plant varieties should be considered an important part of crop management strategies to increase agricultural production on acid soils and to protect forests around strongly acidified industrial regions. Generation of metal-tolerant plants through genetic engineering has been demonstrated to be a valid approach. For instance, expression of the alpha domain of human metallothionine IA in transgenic tobacco plants confers cadmium resistance (21). The production of transgenic plants with an increased capacity to produce and/or excrete organic acids that chelate and detoxify Al in the rhizosphere is an appealing strategy to produce Al-tolerant plants. The effectiveness of citric acid in alleviating Al toxicity has also been demonstrated by adding citrate to solutions containing toxic levels of Al, which reverses the inhibition of wheat root growth caused by Al (22). Citric acid forms a strong chelate with Al, typified by a stability constant of 5 × 108 M−1, which is about 700-fold greater than the corresponding value for the malate–Al complex (23). Citrate overproduction, therefore, appears to be an ideal candidate to produce Al-tolerant transgenic plants. To test whether citrate overproduction could be achieved in transgenic plants and to assess the impact of elevated levels of citrate on aluminum tolerance, our research team produced transgenic tobacco lines that overexpress the citrate synthase from Pseudomonas aeruginosa in their cytoplasm (24). To produce these plants, a chimeric gene, in which the coding sequence of the P. aeruginosa citrate synthase gene (25) transcriptionally fused to the 35S promoter from the cauliflower mosaic virus, was introduced into the genome of tobacco plants. Biochemical analysis of these transgenic tobacco lines showed that most of them had elevated levels of citrate synthase and that they contained in their roots 10-fold higher levels of citrate and exuded five times more of this organic acid into the rhizosphere than did their nontransformed siblings. Because the evidence for the role of organic acid excretion in aluminum tolerance is rather indirect, it was important to determine whether the lines with elevated levels of citrate synthesis and excretion are less or equally susceptible than wild-type plants to phytotoxic concentrations of Al. It was observed that the inhibition of root growth by phytotoxic concentrations of Al is significantly lower in the citrate synthase overproducing lines than in the control (24). To test whether the same strategy could be used in other plant species, the chimeric gene encoding the bacterial citrate synthase was used to transform papaya plants, a crop that is grown in tropical areas where aluminum toxicity limits its cultivation. It was found that transgenic papaya plants expressing the bacterial enzyme developed roots at concentrations of up to 150 mM Al, whereas the controls failed to do so in concentrations above 50 mM (24). The finding that in two different plant species an increased capacity to produce and excrete citrate led to Al tolerance suggests that this strategy might be useful in many different plant species. The production of Al-tolerant plants is just one example of what plant biotechnology could do to improve productivity in developing countries. Drought-tolerant plants or plants with an enhanced capacity to take up nutrients that are present in tropical soils, but that are not readily available for plant nutrition are examples, among others, of technology that could be produced by genetic engineering means, and that could significantly elevate productivity. Transfer of Technology to Developing Countries. Most of the available technology for producing improved transgenic plant varieties could effectively be used to improve productivity in developing countries. Because most, if not all, of these technologies have been patented and belong to private corporations, a major challenge is to identify and establish the mechanisms to effectively transfer this technology to developing countries. Several avenues could be followed: one would be the training of scientists from developing countries in universities, research institutes, and companies in developed countries; a second one is to assist developing countries in establishing their own facilities for biotechnological research; and the third one is to transfer technology, by means of gene constructs or transgenic plants, from universities or companies to the existing research centers in the developing world.

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In terms of training and capacity building, several foundations and government agencies have important programs. Good examples of successful programs of this kind are the rice and cassava programs of the Rockefeller Foundation, the program of the Biotechnology Action Council of the United Nations Educational, Scientific and Cultural Organization (UNESCO) and the International Cooperation (INCO) program of the European Commission, among others. In particular, the success of the Rockefeller rice biotechnology program can be highlighted, which in a few years stimulated biotechnological research for this crop in the U.S. and Europe and facilitated the establishment of rice molecular biology research in many laboratories in many countries in the developing world. In the short term, the direct transfer of technology may be the most effective strategy to implement plant biotechnology to increase productivity in the developing world. Technology transfer can be done by using end products (transgenic seed) that have been developed for the agriculture of advanced countries. Transfer of end products in some cases will be done anyhow if the market is of value to the companies; however, the use of such seed will probably be limited to intensive agriculture of a nature similar to that for which the transgenic seed was originally developed. It would be more interesting if transgenic seeds were transferred to national breeding programs, which could be used as the basis for developing local varieties better suited to local environment and soil conditions. Another possibility is to transfer gene constructs to research institutes that have the capacity to introduce this genetic material into local crops or varieties. How to achieve this is still not completely clear, but a number of mechanisms are beginning to be explored. Transferring this technology has some problems; for instance, when royalties can be waived and when not. Perhaps a naive approach would be to reach agreements in which the technology is donated on a royalty-free basis if it will be used only for production aimed at internal markets of developing countries. In cases where export is possible, royalties should of course be paid; if the farmers can export their products, however, they should at least have certain capacities to share their increased income with the providers of the technology. To be able to meet the needs of developing countries with technology available in public and private institutions in developing countries, a source of easily accessible information will be needed, which preferentially indicates which institutions or companies agree in principle to donate technology. Initial attempts in this direction have been carried out by the International Service for the Acquisition of Agrobiotech Applications (ISAAA). This nonprofit organization is attempting to play the role of an “honest broker,” identifying needs in their target countries and assisting a national institution to reach an agreement with the companies that have the technology that can potentially solve the problem. An example of this is the agreement between the Centro de Investigación y Estudios Avanzados in Mexico and Monsanto to develop virus-resistant potatoes for the Mexican market (26). Having a company as a partner makes it more likely that all the steps, from basic research to field evaluation, are carried out successfully. These still-limited initiatives should be significantly enhanced to make sure that plant biotechnology is transferred to developing countries at an adequate pace. To ensure effective technology transfer, each recipient country must have a research center with the capacity to assimilate the technology and apply it to local crops or local varieties. Although several developing countries, such as Brazil, Argentina, India, and China, have at least some of this capacity, it is clear that not all developing countries have research institutes with sufficient infrastructure and trained personnel to effectively participate in this process. It is therefore urgent that the countries that do not have such capabilities give priority to the establishment of research groups, as well as the regulatory bodies required to assess and approve the use and commercialization of genetically modified organisms. Even if technology is successfully transferred to developing countries and transgenic varieties are developed for local crops, the problem of getting this technology to the small farmer is still an important challenge. The government of each country needs to implement a system for producing and distributing transgenic seeds and any other input, at low or no cost, to the small farmer. Whether technology transfer to developing countries takes place will, of course, depend on the political will of each national government and the resources required. The work on acid soils in my laboratory was carried out with support of the Howard Hughes Medical Institute and the Rockefeller Foundation. I thank June Simpson for critically reviewing this manuscript. 1. James, C. (1997) Int. Ser. App. Agro. Apply Briefs 5, 1–20 . 2. Van Schoonhoven, A. & Voysest, O. (1980) in Bean Production Problems in the Tropics, eds. Schwartz, M. & Pastor-Corrales, J. (Centro Internacional de Agricultura Tropical , Cali, Colombia), 2nd Ed. pp. 33–58 . 3. U.S. President’s Advisory Committee Report (1967) , pp. 20–45 . 4. Food and Agriculture Organization (FAO) (1991) World Soil Resources Report 66 . 5. Buringh, P. , van Haenst, H. D. & Staring, Y. (1975) J. Exp. Bot. 24, 1189–1195 . 6. Von Uexküll, H. R. & Mutert, E. (1995) Plant Soil 171, 1–15 . 7. Dunal, R. (1988) in Management and Fertilization of Upland Crops in the Tropics, ed. Wang, Y. (Nanjing Institute of Soil Science , Nanjing, China), pp. 1–5 . 8. Kennedy, I. R. (1986) in The impact on the Environment of Nitrogen and Sulfur Cycling, ed. Kennedy, I. R. (Cambridge Univ. Press , Cambridge, U.K.), pp. 34–92 . 9. Pandey, S. , Ceballos, H. , Granados, G. & Knapp, E. (1994) in Stress Tolerance Breeding: Maize That Resist Insects, Drought, Low Nitrogen and Acidic Soils. Maize Program, A Special Report, eds. Edmeades, G. E & Deutsch, J. A. (Centro Internacional de Mejoramiento de Maíz y Trigo , Mexico D. F.). 10. Brenes, E. & Pearson, R. W. (1973) Soil Sci. 116, 295–302 . 11. Lopes, A. S. & Cox, F. R. (1977) Soil Sci. Am. J. 41, 743–747 . 12. Saigusa, M. , Shoji, S. & Takahashi, T. (1980) Soil Sci. 130, 241–250 . 13. Kochian, L. V. (1995) Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 237–260 . 14. Haug, A. (1984) CRC Crit. Rev. Plant Sci. 1, 345–373 . 15. Miyasaka, S. C. , Buta, J. G. , Howell, R. K. & Foy, C. D. (1991) Plant Physiol. 96, 737–743 . 16. Delhaize, E. , Craig, S. , Beaton, C. D. , Bennet, R. J. , Jagadish, V. D. & Randall, P. J. (1993) Plant Physiol. 103, 685–693 . 17. Delhaize, E. & Ryan, P. R. (1995) Plant Physiol. 107, 315–321 . 18. Pellet, D. M. , Grunes, D. L. & Kochian, L. V. (1995) Planta 196, 788–795 . 19. Ma, J. F. , Zheng, S. J. & Matsumoto, H. (1997) Plant Cell Physiol. 38, 1019–1025 . 20. Ma, J. F. , Zheng, S. J. , Matsumoto, H. & Hiradate, S. (1997) Nature (London) 390, 569–570 . 21. Pan, A. , Tie, F. , Duau, Z. , Yang, M. , Wang, Z. , Li, L. , Chen Z. & Ru, B. (1994) Mol. Gen. Genet. 242, 666–674 . 22. Ownby, J. D. & Popham, H. R. (1989) J. Plant Physiol. 135, 588–591 . 23. Suhayda, C. G. & Haug, A. (1986) Physiol. Plant. 68, 189–195 . 24. De la Fuente, J. M. , Ramírez-Rodríguez, V. , Cabrera-Ponce, J. L. & Herrera-Estrella, L. (1997) Science 276, 1566–1568 . 25. Donald, L. J. , G. F. Molgat & Duckworth, H. W. (1989) J. Bacteriol. 171, 5542–5550 . 26. Rivera-Bustamante, R. (1997) in Plant Biotechnology Transfer to Developing Countries, eds. Altman, D. & Watanabe, S., R. G. (Landes , Austin, TX).

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

From pre-Hispanic to future conservation alternatives: Lessons from Mexico

ARTURO GÓMEZ POMPA * AND ANDREA KAUS Department of Botany and Plant Sciences and Institute for Mexico and the United States, University of California, Riverside, CA 92521-0124 ABSTRACT In this paper, we review some past and present trends in biodiversity conservation in Mexico and explore possible explanations of why, in spite of this long history of depredation and ineffective conservation policies, the ecosystems have been able to cope with and retain most of their biological components. We suggest a hypothesis based on the persistence of a complex mosaic of past and present traditional land uses as a possible explanation for this resilience. We propose an agenda for the scope of future conservation research and policy, particularly the need to take the socioeconomic context of environmental degradation into account. We put forth a series of questions that we think need to be investigated if the conservation research community is to participate in developing solutions for the future welfare of the human species and of biodiversity on earth. In 1995, Mexico had 94 million inhabitants with a growth rate of 2.1% per year (1). In the last 50 years, Mexico has lost most of its mature humid rain forests, and at 500 to 800 thousand hectares of forest lost per year, it has one of the highest deforestation rates in Latin America (2). Most of its rivers are polluted, and many parts of the country suffer from water shortages. Immense areas show environmental degradation and biological impoverishment. In addition, income distribution among the nation’s citizens is remarkably polarized, with more than 50% of the population living at the poverty level, 20% at the extreme poverty level, and a small group of individuals who are among the richest people on earth (3). In this context, it is striking that Mexico is also one of the most biologically diverse countries of the world (4, 5). It has a wealth of raw natural resources, such as oil, timber, range land, and minerals. The nation has adopted and developed various conservation models to establish systems of national parks, wildlife refuges, watershed protected areas, marine sanctuaries, world heritage sites, botanical and zoological gardens, and biosphere reserves (6). The country contains an impressive number of conservation groups and a well recognized ecological scientific community that has influenced the development of a large system of recently protected areas now covering more than 10% of the nation’s territory. In addition, Mexico is a site where remarkable cultures have developed, flourished, and collapsed over the last 3,000 years. The nation boasts an impressive cultural diversity, with more than 8 million people belonging to more than 50 cultures (ref. 7 and www.ine.gob.mx/ gacetas/gaceta38/pma12.htm ). It has a wealth of empirically based conservation practices stemming from the traditions of indigenous cultures, dynamic and modern descendants of customs that predate Spanish contact. Along with these cultures and practices, Mexico has an impressive number of resilient ecosystems that have coevolved with human activities over thousands of years (8). Despite this seeming cornucopia of biological, ecological, and cultural diversity, Mexico has not been able to slow present trends of environmental degradation and destruction. Biodiversity losses, however, have not reached predicted levels. In this paper, we examine past and present conservation actions and trends to explore why—in spite of a record of depredation and ineffective conservation policies—the country’s ecosystems have been able to adjust and retain most of their biological components. Conservation as Sustainable. In the last few decades, development—the former antithesis of conservation—has come to encompass concepts of sustainable land and resource use to ensure that development “meets the needs of the present without compromising the ability of future generations to meet their own needs” (9). This concept coincides with the broad concept of conservation championed by Aldo Leopold (10) and followed by most conservation organizations today. In this paper, however, we suggest a subtle permutation of the definitions of sustainable development and conservation to encompass those actions that provide environmental and biological safeguards for future generations without compromising the needs of present ones. We believe that the world must realize fully its responsibilities and commitment to the individuals and communities of today who, by design or default, maintain the natural resources on which we all rely. In addition, conservation that sacrifices basic human needs at present for those of the future is fundamentally unjust. It provokes righteous resentment among local inhabitants and escalates boundary disputes at the edges of protected areas, an inherently unsustainable approach to biodiversity protection. The environmental dilemma has become increasingly complex with each successive wave of human expansion, technological advance, and consequent environmental changes. Each change brings on a new set of circumstances to confront and a new sense of urgency as local problems take on global proportions and vice versa. Neither national conservation policies nor local practices have resolved rural development demands or reduced current threats to biodiversity, rampant poverty, and resource depletion. In fact, conservation in Mexico sharply reflects the separation of national policy from the interests of rural communities, as well as the chronic neglect and submergence of indigenous and peasant populations (11). Modern Descendants of Pre-Hispanic Approaches. Research and public opinion regarding native peoples is filled with conflicting perceptions regarding their impact on the environment. Early native Americans are blamed for the extinction of megafauna (12) but are acclaimed for their skillful management of forests and wildlife (13, 14). For example, the Maya civilization, one of the most successful and well known cultures in tropical America, fed and sustained

*To

whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org.

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human populations over many centuries in a tropical environment at numbers and densities well beyond those found in the same place today. However, researchers also claim that the Maya overexploited their environment because of overpopulation (15). The common perception is that Maya mismanagement of forest resources led to the civilization’s ultimate collapse about 1,100 years ago (16). The most recent explanation for the collapse of the Maya comes from Hodell, Curtis, and Brenner (17) who suggest that a prolonged dry-period event in the region coincided with the collapse of the classic Maya. It seems that the ecological basis of the Maya’s highly efficient food-production technology disappeared as a result of a climatic change. The survivors from this period continued their activities in the same region and began a new cycle of population growth that lasted 600 years until the arrival of the Spanish. Far from a pristine environment, the first explorers found a forest region that was densely populated. Cristobal Colon described Hispaniola (Haiti and the Dominican Republic) and Tortuga as densely populated and “completely cultivated like the countryside around Cordoba” (18). Although the evidence indicates that the two cycles of population growth profoundly affected the environment and altered the composition of the forest vegetation, there is no record of any major floristic changes in the lowland Maya region caused by the ancient—or the modern— Maya. The few studies available on the vegetation history of the lowland Yucatecan Maya area, as suggested by the palynological record in lakes, show no major changes in floristic composition at a genus level in the last 5 to 6 thousand years. In fact, the data indicate that the Maya were able to maintain a managed mosaic of forested and agricultural areas simultaneously, as they do today, without an apparent decrease in biodiversity (19). There is no evidence of any major biological collapse, only of a population collapse. There must be an explanation for the unchanged flora in the Maya lowlands in the last 5 to 6 thousand years. There is no evidence (archaeological, historical, or iconographic) of areas purposefully dedicated to preservation in the Maya region, such as sacred groves or untouched reserve sites in other regions of the world (20), with the exception of the sacred cacao groves in sinkholes (21). However, we have learned that in between ceremonial sites and dense rural settlements, there were areas of less-managed forests, complex agroforestry systems, and abandoned agricultural land with secondary vegetation such as we find today (22–24). This managed mosaic was—and remains—the provider of important niches for a large number of organisms. They are “keystone” sites for the recovery of biodiversity after abandonment. It is as much a clue to the conservation practices of the ancient Maya as it is a key for the present. The Maya are not unique in this regard. Ecological and anthropological evidence indicates that many other indigenous groups in different geographic regions had their own approaches to natural resource management that resulted in deliberate or de facto conservation strategies (8, 25, 26). Each group in each geographical site was able to manage its resources with the knowledge accumulated over millennia and under different population pressures; however, we do not want to suggest that aboriginal populations have not also overexploited particular resources or degraded their environments. It is the range of indigenous transformations of the environment, from conservationist to exploitative, from high to low population densities, that needs to be understood if the past is to provide an informed perspective for the future. Two Mexicos. The New World was peopled by civilizations that were not understood by the Spanish; subsequently, these civilizations were decimated, weakened, and suppressed by arms, religion, and disease. Mexico was depopulated, and immense areas were abandoned to undergo natural regeneration. Two Mexicos, indigenous Mexico and colonial Mexico, emerged, and they coexisted and intermingled for nearly 4 centuries, albeit one was subjugate to the other. The former was comprised of the rural, still largely indigenous population descendent from pre-Hispanic cultures; the later was what Bonfil (11) calls “México imaginario,” a minority but dominant society structured around the norms, aspirations, and beliefs of Western civilization. Today, however, the two Mexicos overlap geographically, as mass production techniques of forestry and agribusiness clash with smaller local practices, many of them based on traditional systems of shifting agriculture. Remote no longer means removed. Bulldozers and chain saws cut into formerly isolated regions. Cattle graze over former milpas. Ranches displace rancherías. Subsistence agriculture merges the traditional milpa with livestock production, and valuable natural resources are exported to far-off urban centers. However, a basic division remains between the two Mexicos with respect to policy and regulation. One is the oft-forgotten rural Mexico, a locus of poverty and also a well recognized “keeper of the forest.” The other is the Mexico of national policy and global commerce, which is the financial “miracle” or “disaster” and also the major force behind resource depletion. Even though local natural resource management practices, whether ancient remnants or recent inventions, have been the focus of intensive ethnoecological, ethnobotanical, and anthropological research for many decades, the scientific community still has only an inkling of how local populations interact with the natural environment. It has been even less successful in transferring this understanding to modern conservation policy. However, we caution against the trap of seeing conservation issues as only a distinction between indigenous or Western approaches. Not only would this view be simplistic, it contains the danger of setting indigenous populations and approaches apart from other local populations and land-use practices. Such a dichotomy runs the risk of reincarnating a contemporary version of romantic primitivism regarding indigenous society (27, 28) and placing other local peoples in categories of lesser worth (29). Human land-use practices change depending on circumstances. Decisions to change are based on an empirical understanding of the environment, which, in turn, has different degrees of historical continuity in that particular area. The distinction we wish to make here instead is between local conservation practices, based on a deep understanding of a particular site, and national policies, based on a broad understanding of wider impacts and external threats. National Conservation Strategies. Modern Mexico, the inheritor of colonial Mexico’s philosophies, has taken a progressive approach to conservation, following the trend initiated in the United States at the end of last century by creating different kinds of parks and other national protected areas throughout the country. More than 500 protected areas have been declared officially in the last 80 years, covering more than 50% of the nation’s territory. Unfortunately, the majority of them are “paper parks”—parks in name only—and do not exist anymore. Today, the nation recognizes the decrees of 111 protected areas, which cover close to 10% of the territory (Table 1). A system of protected areas represented perhaps a visionary move for the country, but the government has treated these sites as if they exist in a vacuum, unperturbed by human intervention or ecological change. It presumed the absence of humans before the establishment of the parks, land tenures issues were not resolved, and plans or funds for management were mostly nonexistent. As paper parks, however, the sites protected the environment by dint of their legal status and the low population densities in the regions when they were established. The government discovered one of the unfortunate

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truths regarding the protection of nature in most developing countries: “Decrees cost nothing, they hurt no one and provide adornment; and in some cases, they even protect nature” (6). Unfortunately this problem exists in many other tropical countries (30).

Table 1. Active protected areas of Mexico, 1998 No. Category of protected area Biosphere reserve 21 National park 63 Natural monument 3 Natural resources area 7 Area of flora and fauna 9 In process 8 111 Total

Area, hectares 8,115,730 1,385,334 13,023 203,439 1,660,502 418,941 11,796,969

Percentage of total protected area 68.8 11.7 0.1 1.7 14.1 3.6 100

Data were provided by the Consejo Nacional de Areas Protegidas. In 1977, Mexico became one of the first and few countries to adopt and develop the biosphere reserve system proposed Man and the Biosphere Program of the United Nations Educational Science and Cultural Organization. Mexican scientists felt that science, rather than urban sentiment or a sense of aesthetics, needed to be the basis of environmental protection for human and ecological welfare alike. They thought that the biosphere reserve concept would be a good solution, reconciling the contradictions of overlapping land use and conservation goals. In many ways, Mexico took the lead for developing countries, particularly in the effort to include local people and local needs in the biosphere reserve management and research (31–34). Despite the success of surface area coverage and increased research opportunities, the basic principles underlying the biosphere reserve concept have not been followed, and the reserves suffer from the same problems of neglect and mismanagement as do national parks. We do not want to suggest that the idea of protected areas or the biosphere reserve concept in themselves were wrong, but they have had little chance of working implemented as they were. Beyond their establishment, little was done to maintain or manage biosphere reserves or other forms of protected areas. That is, the only management “decision” was to keep the areas as they were, in the hands of the people living there. In that serendipitous “action” perhaps lies the real success of the biosphere reserve. Beyond Protected Area Management. How can the different Mexican approaches to conservation—one that is based on local empirical knowledge and another that is based on national policy—be reconciled to face current and future threats to the environment? Neither by itself is enough. National policies have been unable to stop trends of deforestation, deterioration, desertification, and resource depletion. These alarming trends continue despite the fact that over 50% of the country’s surface area has been under some form of environmental protection at one time or another (6). In part, the problem is that conservation programs are designed and implemented without understanding or accommodating local needs and aspirations. Local traditional practices are not the “silver bullet” for conservation either. They are site-specific, were developed under earlier environmental conditions, and cannot control for externalities that arise from global demands and free market policies as well as local demands from a growing population. For instance, timber in the Yucatán peninsula does not supply the population centers there; instead, it goes to build houses and furniture in Europe or the United States or railroad ties in Mexico. Worse yet, the timber goes unprocessed; thus, its highest value as lumber is exported as well. In turn, the integration of conservation and development as a legacy of the biosphere reserve concept has not succeeded in the manner that it was intended either. Funding agencies, convinced that this approach is the answer, have poured money into such programs without thinking out the details or consequences. In trying to meet development needs, well meaning conservation programs often lose sight of the link between development and environmental protection (35). Focus may be placed on peripheral activities such as certain agriculture techniques, handicrafts, or cottage industries without making the explicit connection to reduction of deforestation and other environmental pressures or taking into consideration the perspectives of the local land users (36). So what is the answer? Who has an answer at all, and what is the appropriate and ethical level for making decisions about future conservation practices? Out of this morass of failed and half-tried conservation options, several things seem clear. First, protecting surface area is not enough. Today’s conservation sites are faced with the basic needs and rights of local populations for food, water, shelter, and fundamental social services. In addition, these sites are subjected to the demands of a world that is hungry for raw resources and the demands of a country that must balance economic debt against environmental protection and that depends on the subsidies of nature to do so. Relying on the encirclement of wilderness to meet conservation needs now or in the future is short-sighted, regardless of how we personally feel about the need for untrammeled wild places. Second, if predictions of large climatic shifts are correct, these sites may not be located in critical areas for the conservation of biodiversity. Conservation requires the management and preparation for change, not the maintenance of the status quo. We need to emphasize ex situ as well as in situ conservation efforts to keep the basic building blocks of biodiversity for future restoration. Third, we need to find where conservation is, instead of where it is not. We do not tend to hear about places where outside intervention is unnecessary because of isolation or because of the proactive efforts of local communities or individuals. These are the very places we actively need to seek out, study, and compare to understand what conditions lead to a local conservation ethic. In isolation, such small local actions may seem insignificant, particularly in the face of global-scale pressures, but in sum, local action may hold the basic building blocks for developing conservation programs elsewhere. Fourth, conservation on a larger scale needs to be based on vertical partnerships between and the mutual accountability of local communities and the nation. Local communities have detailed knowledge of particular sites, whereas national levels have a larger vision and stronger authority. Local communities need to have the ability to hold the nation accountable to their rights, including decisions regarding their resources, but the nation needs to retain the responsibility to watch over the use of critical resources, habitats, and ecosystems (37). Fifth, rather than focus on population numbers alone, we need to recognize and hold accountable those sectors of the human population that are the key extractors of resources. The growth of the cattle herds, the extent of the agricultural frontier, and the amount of timber harvesting all respond to consumptive demands for beef, produce, wood, and paper products from burgeoning and pampered populations far removed from the supply source. All the terracing, green mulching, selective harvesting, field rotation, crop diversity, and reforesting in the world cannot help if the external consumption of natural resources continues to outpace local sustainable practices and to offer economic incentives that out-compete long-term conservation benefits. Is such a scenario for effective conservation research utopian? No. Many of these objectives are being explored by several grass roots organizations all over the world. In Mexico,

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for example, a small nongovernmental organization, the Programa de Acción Forestal Tropical (PROAFT), with which we have worked since its inception, provides a good example of this trend. Its basic approach is to recognize, encourage, and promote conservation actions of rural communities. Every year, participant communities present their accomplishments and new ideas with members and guests. In these meetings, visits are arranged; problems are presented; and initiatives are suggested by participants. What has been accomplished is a three-way learning process to understand methods for biodiversity conservation, for reinforcing local cultural values, and for dealing with a market society (38). One PROAFT project undertaken recently by a group of Mixtec peasants from the organization Ecosta Yucui Cuii initiated the creation of a new type of protected area: the “Cellular Campesino Reserve.” Each participant contributed a piece of their land—a “cell”—ranging in size from 0.5 to 15 hectares. The total amount of protected area is 167 hectares within an area of more than 2,000 km2. Hopefully, this step is only the beginning. The campesinos believe that this approach to conservation is more realistic; everybody participates, and all are the protectors of their cells. This approach may mimic a hypothetical conservationist approach of ancient cultures, which would have set up patches of “leftalone” forests throughout the environment from which biodiversity was able to regenerate after abandonment. PROAFT is not unique. It is encouraging to see that, throughout the world, innovative programs and ideas are arising that directly confront the intertwined problems of ecological and social welfare under the threat of overpopulation (39). Community-based conservation and comanagement regimes are no longer fringe efforts but part of mainstream trends within research and conservation communities alike. Future Solutions or Future Questions? Before this century of technological and population explosion, people were not as overtly aware or concerned about the need to conserve resources as we are. They relied on the inherent capacity of ecosystems to come back after disturbance. They counted on environmental resilience. The most intriguing support for this resilience hypothesis is our inability to find examples of major mass plant extinctions in the tropics. Rare or endangered species in highly disturbed regions, such as Veracruz and Yucatán, have been found in isolated forest patches in rural areas and in traditional agroforestry systems or other human-impacted systems, such as along roads, in secondary vegetation, or in the few protected areas (40). The predicted massive extinctions in Mexico have not occurred (41). Is it because we do not have recent surveys? Or is it because we have an unknown system of patches (natural and artificial) where most species hang on in de facto “refuges” until a new human population collapse occurs and ecological regeneration begins one more time? Is the managed mosaic the only option left to face the natural or human threats to biodiversity and human survival? And what happens if the patches disappear? Are we teetering on the edge of nature’s resilience? Of course, we need to explore what nature’s resilience means in highly populated countries such as India, Rwanda, Mexico, the Netherlands, and Japan. It seems that this exploration will be the real challenge for the next century. We know that nature has proven its capacity to recuperate under changing conditions. However, humans are running out of time to resolve the obscene inequalities in our societies that go hand in hand with the present state of resource use and conservation and with the disturbing fact that millions of people today are undernourished and impoverished. We are running out of time to find ways to resolve these inequalities within the present capacity of the environment, and there is even less time considering that this capacity diminishes with increasing population and consumption demands. We are running out of time to convince the world of the urgency to find a new vision for population growth, food production, economic development, resource use, and biodiversity conservation. It is not nature that is running out of time; it is the human species. We thank Vernon Heywood, Brian Haley, Norman Ellstrand, Richard Whitkus, and Scott Fedick for their comments and suggestions. 1. World Resources Institute (1996) A Guide to the Global Environment: The Urban Environment (Oxford Univ. Press , New York). 2. Challenger, A. (1998) Utilización y Conservación de los Ecosistemas Terrestres en México. Pasado, Presente y Futuro (Comm. for Biodiversity of Mexico, Natl. Autonomous Univ. of Mexico, and Sierra Madre , Mexico City). 3. Gómez-Pompa, A. , Kaus, A. , Jiménez-Osornio, J. , Bainbridge, D. & Rorive, V. (1993) Sustainable Agriculture and the Environment in the Humid Tropics (Natl. Acad. Press , Washington, DC), pp. 483–548 . 4. Ramamoorthy, T. P. , Bye, R. , Lot, A. & Fa, J. , eds. (1993) Biological Diversity of Mexico: Origins and Distribution (Oxford Univ. Press , New York). 5. Mittermeier, R. A. & Mittermeier, C. G. (1992) in México Ante los Retos de la Biodiversidad, eds. Sarukhán, J. & Dirzo, R. (Natl. Comm. for Biodiversity of Mexico , Mexico City) , pp. 63–73 . 6. Gómez-Pompa, A. & Dirzo, R. (1995) Las Reservas de la Biosfera y Otras Areas Naturales Protegidas de México (Secretary of the Environ., Nat. Resour. and Fisheries of Mexico, and Comm. for Biodiversity of Mexico , Mexico City). 7. Bye, R. (1993) in Biological Diversity of Mexico: Origins and Distribution, eds. Ramamoorthy, T. P. , Bye, R. , Lot, A. & Fa, J. (Oxford Univ. Press , New York), pp. 707–731 . 8. Gómez-Pompa, A. & Kaus, A. (1989) in Alternatives for Deforestation, ed. Anderson, A. (Columbia Univ. Press , New York), pp. 45–64 . 9. World Commission on Environment and Development (1987) Our Common Future (Oxford Univ. Press , New York). 10. Flader, S. L. & Callicott, J. B. , eds. (1991) The River of the Mother of God and Other Essays by Aldo Leopold (Univ. of Wisconsin Press , Madison, WI). 11. Bonfil, G. (1987) México Profundo (Editorial Grijalbo , Mexico City). 12. Martin, P. S. & Wright, H. E., Jr. , eds. (1967) Pleistocene Extinctions: The Search for a Cause (Yale Univ. Press , New Haven, CT ). 13. Voorhies, B. (1996) in The Managed Mosaic: Ancient Maya Agriculture and Resource Use, ed. Fedick, S. L. (Univ. of Utah Press , Salt Lake City), pp. 17–29 . 14. Cronon, W. (1983) Changes in the Land: Indians, Colonists, and the Ecology of New England (Hill & Wang , New York). 15. Rice, D. , Rice, P. M. & Deevey, E. S. (1985) in Prehistoric Lowland Maya Environment and Subsistence Economy, Papers of the Peabody Museum of Archaeology and Ethnology , ed. Pohl, M. D. (Harvard Univ. Press, Cambridge, MA), Vol. 77 , pp. 91–105 . 16. Abrams, E. M. , Freter, A. C. & Rue, D. J. (1996) in Tropical Deforestation, eds. Sponsel, L. E. , Headland, T. N. & Bailey, R. C. (Columbia Univ. Press , New York), pp. 55–75 . 17. Hodell, D. A., Curtis, J. H. & Brenner, M. (1995) Nature (London) 375, 391–394 . 18. Denevan, W. (1992) Ann. Assoc. Am. Geogr. 82, 369–385 . 19. Dunning, N. , Beach, T. & Rue, D. (1997) Ancient Mesoam. 8, 255–266 . 20. Gadgil, M. & Chandran, M. D. S. (1992) Indigenous Vision: Peoples of India Attitudes to the Environment (India Int. Cent. Q. , New Delhi), pp. 183– 187 . 21. Gómez-Pompa, A. , Flores-Guido, J. S. & Aliphat, M. (1990) Lat. Am. Antiquity 1, 247–257 . 22. Atran, S. (1993) Curr. Anthropol. 34, 633–700 . 23. Fedick, S. L. (1996) in The Managed Mosaic: Ancient Maya Agriculture and Resource Use, ed. Fedick, S. L. (Univ. of Utah Press , Salt Lake City), pp. 107–131 . 24. Gómez-Pompa, A. (1987) Mex. Stud. 3, 1–17 . 25. Alcorn, J. B. (1984) Huastec Maya Ethnobotany (Univ. of Texas Press , Austin, TX).

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26. Baleé, W. L. (1994) Footprints of the Forest: Ka’apor Ethnobotany—the Historical Ecology of Plant Utilization by an Amazonian People (Columbia Univ. Press , New York). 27. Pearce, R. H. (1988) Savagism and Civilization: A Study of the Indian and American Mind (Univ. of California Press , Berkeley, CA). 28. Redford, K. H. (1990) Orion 9(3) , 25–29 . 29. Dasmann, R. F. (1984) in National Parks, Conservation, and Development, eds. McNeely, J. A. & Miller, K. R. (Smithsonian Inst. , Washington, DC) , pp. 667–671 . 30. Van Schaik, C. P. , Terborgh, J. & Dugelby, B. (1997) in Last Stand: Protected Areas and the Defense of Tropical Diversity, eds. Kramer, R. , van Schik, C. & Johnson, J. (Oxford Univ. Press , New York) , pp. 64–89 . 31. Halffter, G. (1984) in Ecology in Practice, eds. di Castri, F. , Baker, F. W. G. & Hadley, M. (Tycooly Int. and United Nations Educ. Sci. and Cultural Organ. , Dublin) , Vol. 1 , pp. 428–436 . 32. Halffter, G. (1988) in Estudio Integrado de los Recursos Vegetación, Suelo y Agua en la Reserva de la Biosfera de Mapimí, ed. Montaña, C. (Inst. de Ecol. , Mexico City) , Vol. 23 , pp. 19–44 . 33. Kaus, A. (1992) Dissertation (Univ. of California , Riverside, CA). 34. Kaus, A. (1996) in Strategies for Conservation of the Sierra San Pedro Martir, eds. Franco Vizcaíno, E. , de la Cueva, H. & Montes, C. (Cent. de Invest. Científica y Educ. Superior , Ensenada, Mexico) , pp. 1–3 . 35. Brown, M. & Wyckoff-Baird, B. (1992) Designing Integrated Conservation & Development Projects (Biodiversity Support Program/World Wildl. Found. , Washington, DC). 36. Brandon, K. (1997) in Last Stand: Protected Areas and the Defense of Tropical Diversity, eds. Kramer, R. , van Schik, C. & Johnson, J. (Oxford Univ. Press , New York) , pp. 90–114 . 37. Wyckoff-Baird, B. & Kaus, A. (1999) in The Power of Nature: Negotiating Decentralization Processes for Biodiversity Conservation (Biodiversity Support Program/World Wildl. Found. , Washington, DC) , in press . 38. del Amo, S. , Gómez-Pompa, A. , Roldan, A. & Kaus, A. (1993) in Agroecología, Sostenibilidad y Educación, eds. Ferrera Cerrato, R. & Quintero Lizaola, R. ( Cent. de Edafología, Colegio de Postgraduados , Montecillo, Mexico) , pp. 8–18 . 39. Gadgil, M. (1998) in Linking Social and Ecological Systems, ed. Berkes F. & Folke C. (Cambridge Univ. Press , Cambridge, U.K.) , pp. 30–47 . 40. Sosa, V. & Platas, T. (1998) Conserv. Biol. 12, 451–455 . 41. Gómez-Pompa, A. , Vázquez-Yanes, C. & Guevara, S. (1972) Science 177, 762–765 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Gardenification of tropical conserved wildlands: Multitasking, multicropping, and multiusers

DANIEL JANZEN * Department of Biology, University of Pennsylvania, Philadelphia, PA 19104 ABSTRACT Tropical wildlands and their biodiversity will survive in perpetuity only through their integration into human society. One protocol for integration is to explicitly recognize conserved tropical wildlands as wildland gardens. A major way to facilitate the generation of goods and services by a wildland garden is to generate a public-domain Yellow Pages for its organisms. Such a Yellow Pages is part and parcel of high-quality search-and-delivery from wildland gardens. And, as they and their organisms become better understood, they become higher quality biodiversity storage devices than are large freezers. One obstacle to wildland garden survival is that specific goods and services, such as biodiversity prospecting, lack development protocols that automatically shunt the profits back to the source. Other obstacles are that environmental services contracts have the unappealing trait of asking for the payment of environmental credit card bills and implying delegation of centralized governmental authority to decentralized social structures. Many of the potential conflicts associated with wildland gardens may be reduced by recognizing two sets of social rules for perpetuating biodiversity and ecosystems, one set for the wildland garden and one set for the agroscape. In the former, maintaining wildland biodiversity and ecosystem survival in perpetuity through minimally damaging use is paramount, while in the agroscape, wild biodiversity and ecosystems are tools for a healthy and productive agroecosystem, and the loss of much of the original is acceptable.

THE WILDLAND GARDEN Tropical wildlands and their biodiversity will survive in perpetuity only through their integration into human society. One protocol for integration is to explicitly recognize conserved tropical wildlands as wildland gardens (1, 2). Gardens—space and circumstances for our domesticates, the engineered living extensions of our genome—are an integral part of Homo sapiens. Garden terminology, acceptance, perception, administration, and usefulness are deeply imbedded in our genetic and cultural codes (e.g., refs. 3 and 4 ). This conservation protocol is meant to explicitly apply a profound and positive portion of humanity to what has been largely viewed as “the enemy” throughout humanity’s existence. In the domestic garden—the clothing of the agroscape— select and selected organisms are ordered and tended for perceived optimal harvestable productivity and priorities by some portion of humanity. In the wildland garden, the ordering and tending is less orderly and more non-human, and is left to run its course. However, the ordering and tending is still an investment by the species that owns Earth. The produce from the domestic garden arrives largely in predictable sacks and boxes, while the produce from the wildland garden, in keeping with its vastly more diverse nature and its incessant revelations, comes in an ever-expanding diversity of forms and containers. And, this diverse produce is delivered, albeit often invisibly and for vastly more numerous uses, to the same array of users that receives the agroscape’s more monotonous produce. This commentary is so generic that it may generate a “ho–hum” reaction. It is, after all, self-evident that if large blocks of selfperpetuating tropical wildland gardens can generate sufficient goods and services for local, national, and international society to be as valued and as possessed as the agroscape, we have taken a giant step toward ensuring their perpetual survival. There are proportions of land use whereby the opportunity cost of a hectare of rice field and a hectare of wildland forest are the same. And, we do not live by bread alone. How does one facilitate nondamaging or minimally damaging development of wildland biodiversity and its ecosystems? By the generation of wildland garden goods and services, and by recognizing this generation at local, national, and international levels. We need to ask less what is the opportunity cost of a wildland and ask more what is the opportunity cost of its urban and agroscape alternatives. Hurricane Mitch’s impact on society was not only a function of the amount of rain and wind it generated. Here, I focus on the “generation” of goods and services from the wildland garden, rather than their “recognition” on the marketplace. But by that distinction, I do not mean in any way to belittle that other major requirement for survival of a wildland garden. If there is no market for soybeans, then society grows corn.

THE WILDLAND YELLOW PAGES A major way to facilitate the generation of goods and services by a wildland garden is to generate a public domain Yellow Pages for the organisms in those wildlands (5). A Yellow Pages is a device that facilitates the use of the concentrated, diverse, and semireplicated offerings of a city. It does not itself decrease the crime rate, provide public transport, maintain the phone system, or generate a hospital or a library. However, it enormously facilitates the movement of goods and services. This leads to more goods and services, and better tracking of human desires by them. And taxes on this movement redistribute income and pay for many essential public services. The newly blossoming internetization of the world allows many kinds of biodiversity and ecosystem Yellow Pages for the wildland garden. A Species Home Page for each species (and if you like, each ecosystem) in a wildland garden is an entry in a Yellow Pages (e.g., http:// janzen.sas.upenn.edu ). This intertwined set of processes in turn allows the emergence of the concept of the green freezer.

*To

whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org.

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A TALE OF TWO FREEZERS As we move through the age of genetic sequencing and see what can be done with a sizeable chunk of a species’ code, it occurs to many to solve the “conservation problem” by plunking into a nitrogen vat a sample of each species. Such a concept generates a blizzard of concern over species ownership (what better indication that some wild things are already viewed by some as being in their gardens?). However, questions of intellectual property rights are not the focus here. I will assume that every frozen vial is unambiguously labeled with place of origin and that the place of origin owns the vial and all that derives from it (just as with my car being parked by the valet in your garage). This brown freezer leads immediately to the concern of “how do you know what was put in the vial?” Again, I will sidestep this issue by taking the futuristic view that “by thy code thy shall be known.” So now we have this immense building filled with immense vats of liquid nitrogen serviced by shivering robots, a building strategically located somewhere at the point of intersection of the superpowers and the not-so-superpowers. It contains samples of each of our 30 million wildland species. Would someone please run us a budget for this building(s)’ care, feeding, insurance, backups, administration, civic civility, politics, and and and? To get more place-based and society-specific, I would like to know the real cost into the real future of the portion(s) of the brown freezer(s) that houses the “235,000” species that creep around in the particular wildland garden that I, Winnie Hallwachs, and many local, national, and international others are attempting to drag, shove, and attract into perpetual survival through nondamaging biodiversity and ecosystem development in northwestern Costa Rica (Area de Conservacion Guanacaste, ACG: http://www.acguanacaste.ac.cr ). As a first cut, I estimate that the annual nonsubsidized storage and retrieval cost is $20 per vial (including amortization of the installation (s) and the costs of all that portion of society associated with it). We are then looking at a minimal annual warehouse bill of $4.7 million. So, now we have two warehouse options. One is a floor in the brown freezer and the other is the 88,000 ha of the ACG green freezer. A Yellow Pages can be created for each freezer (from whence, see below). In the brown freezer Yellow Pages, each species is represented by a sequence and a unique identifier for its vial(s). A few entries will have a URL to a scientific name and from there to what we are all familiar with. In the green freezer Yellow Pages, each species’ entry has an interim or actual scientific name, as well as ever-increasingly, a genetic sequence. Each species has a URL to a Species Home Page that contains, and/or has pointers to, what humanity knows and comes to know about that species (including an ever-increasing number of sequences). As the days and years pass, the Species Home Pages swell and there are more pointers. How are the brown freezer and the green freezer built? In either case, we spent $500 per species right now getting the species in hand, determining that it is different, recording whatever information comes with the sample process, and sequencing some part of the sample. And on to the next species. Over, perhaps, 10 years, $117,500,000 of capital investment is spread. I will assume that the cost of squencing the contents of the vials, once in hand, is vanishingly small (which is where we appear to be headed). But in one case, we send the sample to the brown freezer and walk away, “conservation accomplished” (warehousing accomplished). In the other case, we trash the sample and settle in to increase the value of the green freezer where it stands in the wind and the rain. We set out to find out, and to organize what we find out, about the wildland garden, supported by a $4.7 million annual budget (which we are now not spending on a floor in the nonexistent brown freezer). Now fast-forward several decades. You are the user. You want a sample delivered next week (tomorrow?—well, that costs a little more). From which of these two freezers would you order your sample? If you order from the brown freezer, you get a sequence, and you get the same associated information in hand as at the time it went into the freezer. And in some cases, there are some new URLs for information about that sequence, or new information about that sequence’s species from some surviving population (maybe) somewhere on the globe. If you order from the green freezer, what happens? Your e-mail is taken by one of the staff supported by the $4.70 million annual budget, who in turn examines the Species Home Page for that species on the green freezer’s web site. This indicates which staff member is “green freezer biodiversity librarian” for that taxon and/or habitat. This parataxonomist or paraecologist reads the account, puts on hip boots, climbing gear, or headlamp, and a day later has a fresh sample in hand, floating in any number of possible standard receiving preservatives. Or an emails comes back to you: “sorry, a fresh sample of that species is not available until the dark of the moon (within 15 days), or the beginning of the rainy season (within 11 months), or until we spend 3 days baiting the site with rotten mangos.” Or, “The impossible just costs a bit more than the usual order.” Incidentally, you already knew this because it was part of the Yellow Pages account for that species, part of the Species Home Page for that species. A critical element of sample preparation in the field was that a tiny bit of the purported sample was removed and plunked into a pocketsized gadget that took a sequence. The sequence was radioed into an internet line that carried it to a database and sent back the message that “yes, as believed, what you have in hand is in fact Pseudomyrmex nigrocincta ” or “no, in fact it is Manduca dilucida, last seen 2 km NNW in 1998.” And where did this biodiversity Dewey Decimal system and librarian for the wildland garden come from? About $3.75 million of the $4.75 million is spent annually on systematically capturing ever more natural history, taxonomic security, trappers’ rules, microgeographic locations, and interaction knowledge about those species and depositing that information in the Species Home Pages for those species. Gradually, the wildland garden moves into “more known” status, with its information creating yet more synergy with the same process in other wildland gardens/green freezers. No such synergy exists among the vials, vats, robots, and floors in the brown freezer. Given the way society works, a diminishing percentage of the requests to the green freezer will be for a vial of species X, Y, or Z, and more will be for a sample(s) of “any (several) species” with specific traits. “I need a small annual herbaceous vine that grows on magnesiumrich phosphorus-poor soils, fruits at the end of a 6-month rainy season, has a tuber, and is fed on by caterpillars of the family Sphingidae.” In other words, the search will be for suites of processes or traits, searched for through the accumulated Species Home Pages by both the machine and the human and recast through the eyes of the biodiversity librarian who makes a career at this honorable pursuit of “know thy neighbor.” At one end of the chain, “let your fingers do the walking.” At the other end there is a biodiversity manager/custodian who knows the beasts as does a rare book librarian or a Japanese gardener. And whence the $117.5 million capital investment and the annual $4.7 million for the green freezer, the truly inventoried wildland garden? In short, the same sources as for the brown freezer, the user fees, tax base, and investors that foot the bill for all of the other major sectors of society. Wildland biodiversity, and its ecosystems, and its information, are not free goods.

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I would argue that it is better business for society to invest in green freezers than brown freezers, despite the long and clumsy history of both. Where are the real impediments to such investments? Every day exposes more “unexpected” human obstacles as well as more facilitating technologies, such as the internet and genetic sequencing, and liberating policy movements, such as blossoming of governmental decentralization and government– private interest partnerships.

BIODIVERSITY PROSPECTING Biodiversity prospecting is now a household phrase both inside and outside of the tropics, and its practice has been with us as long as we have been humans (e.g., refs. 6 and 7 ). We all focused on the first word of that pair and the linkage of biology with nondamaging commerce, and thought “Oh how nice.” I still do. Biodiversity prospecting is a nice item to have in the menu of wildland goods and services. But look at the second word. When was the last time you encountered a gold mine that returned its profits to the maintenance in perpetuity of the soil and mineral deposit of the mine? Are mining companies famous for their contributions to national sustainable development and harmony with the environment? Are mines famous for the quality of life of their employees? Is a mine a self-supporting institution with a future and a key role in local, national, and global sustainable development? Does the old man with the pick and the mule serve as a first-class role model for our youth? Something got left out. What got left out is that the function of biodiversity prospecting in conserved wildlands, that thing that a lot of us have put and still put a lot of energy into, is to help the conserved wildland garden pay for its ticket at society’s table. But those guilds in our society that are filled with professionals at prospecting and managing the ore onto the hardware shelf are generally inclined to put the bottom line into very different coffers than the hole in the ground. Venture capitalists love the bottom line, not the object that generates it. There are two challenges in biodiversity prospecting. First is harvesting the crop, and doing it well. We actually know how to do that and are even getting much better at it. And the biodiversity Yellow Pages is part of that prospecting. But the second is bringing home the bacon rather than paying the bar tab with it. We are way behind and getting further behind on this in biodiversity prospecting (e.g., http://www.oneworld.org/cse/html/dte/ ). Biodiversity prospecting will not begin to realize its potential for the wildland garden until the wildland garden itself begins the prospecting process and then partners with the downriver users. The garden needs to place its own Yellow Pages on the internet, answer the call from the client, and write the contract (8, 9). This is not to say that intermediary downriver specialists at data and sample manipulation have no role. However, their role should be to act as a kind of value added rather than view the wildland garden as a mine in which to prospect or a rear patio on which to place the barbecue. The most important part of a biodiversity prospecting project document is not the technology or the intellectual property rights but the administrative protocol whereby the benefits return to the source.

“ENVIRONMENTAL SERVICES CONTRACTS” BETWEEN THE WILDLAND GARDEN AND SOCIETY Environmental services contracts are not new (e.g., ref. 10 ). Water rights and watershed access/protection have been a market commodity for millennia if not tens of millennia. Biodiversity prospecting is based on environmental services contracts, although they are not called that. Every ecotourist has a microenvironmental services contract with the national park at the gate or through the IRS intermediary. Every successful farmer has an unspoken environmental services contract with the domestic plants and animals, paid across a multitude of counters (e.g., ref. 11 ). But there are still huge portions of society and major geographic regions that are living by the law of the frontier, somewhere between getting free goods and having an unpaid environmental credit card bill. We are on the verge of environmental services contracts between the wildland garden and some social sector (e.g., Appendix I and Appendix II ) becoming a blossoming growth area. However, when a wildland garden, as an institution, stands up tall and says, “Hey, when you eat at my restaurant you pay the bill,” much of society is not so very pleased about the new kid on the block (e.g., http://www.oneworld.org/cse/ html/dte/). At the end of the day there are at least three outstanding and deeply rooted disruptive forces. First, a government-based wildland garden (national park, wildlife refuge, biosphere reserve, conservation area, and their multiple permutations) having the sense of self and administrative and technical skills to develop a contract with its clients, be they local, national, or international, is an act of political decentralization and government–private sector partnering that sends shock waves through the highly centralized governments characteristic of tropical “undeveloped” countries (e.g., http://www.oneworld.org/cse/html/dte/ ). These countries are not undeveloped but rather differently developed. It is quite striking that the Global Environmental Facility (GEF) of the World Bank, in its recent book “Valuing the Environment” (12), chose to locate the example of a Costa Rican environmental services contract ( Appendix I ) in a new section termed “beyond government,” which it is, rather than place it in the many other parts of the book focused on environmental services contracts and the valuations in them. Second, many occupants of the agroscape in developing countries are running agrobusinesses on very narrow profit margins, whether measured in barter or in cash. For these occupants to have to pay for environmental services (from a wildland garden or the agroscape itself), services that they currently treat as free goods, will put many out of business. The attendant sociological, economic and political consequences will be blamed on the environmental services contract (just as the impact of Hurricane Mitch is blamed on the hurricane), rather than on the act of living on an environmental credit card and not paying the monthly bill. Charging the user for irrigation and hydroelectric water, biological control agents, erosion control, worker disease prevention, technical information, firewood, biodegredation, carbon storage, seed sources, and many other currently free goods is no different than raising the costs of gasoline, refrigerators, telephones, over-the-counter drugs, barbed wire, pesticides, tractor parts, taxes or labor, or no different than lowering the market price of beef, cotton, fish, melons, or mangos. Attempting to internalize environmental costs quickly reveals that tropical agroscapes established under subsistence and market economies commonplace in 1850 have today far more people on them than can be supported at the standard of living desired by those people. When a tropical wildland garden puts the spotlight on its many services to the countryside so as to be able to directly pay its own rent and meet its own opportunity costs, the process is applauded by those of us generically aiming at sustainable healthy agroscapes and those agrobusinesses that have set their sights on being in a healthy agroscape (e.g., Appendix I and Appendix II ). However, the process is vilified with equal or more intensity by those who are still living on the “frontier” setting for their computer. The conflict between the applauders and the vilifiers may be dressed up as nationalism versus internationalism, socialism versus capitalism, upperclass versus lowerclass, indigenous versus immigrant, etc., but the real bottom line often lies in who determining who will pay the environmental bills. Third, when a conserved wildland garden begins, it generally starts with the crudest attitudes of the “end of the frontier.”

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The park ranger (a.k.a., the police) attempts to prohibit what may be centuries of unrestrained predation and harvest from the wildland commons by the quick and the clever. This tends to lead to the political chaos of the “disenfranchised and their lawyer champions” flailing out at the centralized and somewhat less frontier-like national and international societies that dictated this kind of “conservationist” policy in the first place. Alternatively, there may be true open-market purchase of the conserved wildland garden for that purpose, with its indigenous occupants becoming the garden’s managers or moving on to occupy other guilds. In either path to a wildland garden, the institution is confronted with an angry social force that potentially may be appeased by biodiversity and ecosystem development of the wildland site. Development means budgets, salaries, and training; it means setting up an industry, a green freezer based on skilled labor, a sort of biological Silicon Valley and Library of Congress rolled up into one. And this wildland industry has enormous local growth potential. Why is it generally not welcomed with open arms by even the “local populace?” Because in great part, unless very explicit steps are taken to counter this, the new employees in the factory are neither the newly disenfranchised previous harvesters from that wildland nor their sons and daughters. Ironically, the people most likely to be chosen by virtually any style of job search—the quick, the flexible, the alert, the educated, the curious, the driven—are the least likely to have been those previous harvesters, even if they were born there. Some very explicit affirmative action for “local hiring” (e.g., in the construction of parataxonomists and paraecologists and other kinds of staff; ref. 13) can to some degree restore the balance. However, this in turn is viewed dimly by the centralized portions of national societies, those who themselves see their sons and daughters competing for an ever-shrinking contemporary national resource base. This shrinking is inevitable as a society winds off the frontier and is confronted with a monstrous environmental credit card bill, as well as having few remaining still-mineable (usually unrenewable) natural resources (such as the massive old-growth forests that were liquidated to bankroll the agroscape and urbanity during the past several centuries). And we even revisit the first problem mentioned above: a complex resident staff in charge of its own wildland garden and knowing best how to treat it brings the threat of wresting power of decision and action from the centralized government.

BE POSITIVE How can one design for intrinsic permanence of wildland gardens, a permanence that “just happens?” Human societies are adept at lowering the overhead on the manipulation of individuals and guilds through microgeographic design. Good fences make good neighbors. Stoplights live at intersections. We certainly do not now have design of conserved wildlands for permanence. And I think that a major reason we do not have it now is because the conservationists and the spoilers are both trying to have it all. We need twin philosophies operating on big landscapes. On the one hand, there should be wildland gardens within a generic goal-oriented framework for wildland permanence and on which are hung place-based regulations for a specific garden. These wildland gardens should be as large and as complex as absolutely possible. One framework commandment is that we (society) formally agree to be happy with what survives in them, and to some degree give up on what is outside of them. Another is that they are forever—no bankrupcy allowed. Another is that we recognize that they are ecological islands in a sea of agroscape and always will be. Now let’s get on with making them high-quality islands. On the other hand there is the agroscape, a habitat in which biodiversity is simply one of the tools in the toolbox—albeit a very important one—but not the priority. The priorities are humans and their happiness. Whatever biodiversity and ecosystem traits survive, survive. We are all happy that they do, but biodiversity survival per se is not the driving/shaping force except where that biodiversity is the best tool for a happy agroscape and the people in it, where it is as much a part of the agroscape as a road or cotton plant. Now let’s get on with making it a highquality agroscape. We have had 10,000-plus years of trial and error “successful” agroscapes but only a few decades of practice with the explicit wildland garden. However, when it comes to creating sustainable agroscapes occupied by happy clients, both major kinds of land use are still in kindergarten. Such a landuse macrodichotomy means that we will be happy saving a high percent of, but not all, wild biodiversity for perpetuity. Yes, such a land-use plan is triage. And if something appears in the agroscape that we desperately want to save, the option is very clear. We go out on the real estate market, buy its home, and put it in the wildland garden. Society understands that you get what you pay for. A broad-brush wildland garden protocol such as discussed here will be more applicable to some current landscapes than others. And it means that many small populations will disappear. But I cannot think of any tropical society where the application of such an attitude would not have a calming effect on the contemporary border wars between society and wildland conservation. Second, its application, slow and steady, holds out far more hope to large amounts of extant tropical biodiversity and its ecosystems than does continuation of a cops-and-robbers mindset. If you want to keep the gold under your bed from being stolen, put it to work on the marketplace and diversify your portfolio. I have long believed (3, 14) that conservation of wildland biodiversity and its ecosystems, and their integration with society, are unavoidably and inextricably place-based. The only generic formula is the goal of conservation by means of nondamaging integration with society. The world as a whole will achieve far more wildland conservation in perpetuity by diminishing the planning and pursuit of the “conservation model” and conservation assessment and by putting the very considerable resources currently spent on these stratospheric activities into the specific nondamaging integration of specific large wildlands with specific parts of their societies throughout the tropics. We are not alone in this observation (15).

APPENDIX I (Translated from the Spanish original.) Environmental Services Cooperative Agreement between the Ministerio del Ambiente y Energia, and Grupo Del Oro, S. A., a subsidiary of CDC, in northwestern Costa Rica. Between us, Carlos Manuel Rodriguez Echandi, of legal age, married, attorney at law, identification card number 1529682, resident of San Jose, Costa Rica, in my position as acting Minister of the Ministerio del Ambiente y Energia (MINAE), according to nomination decree 26850P in the Gaceta No. 88, 8 May 1998 and from here on termed “MINAE”, and Norman Justin Braithwaite, of age, married, businessman, U.K. passport 740050714, in his position as President of the Board of Directors of Grupo Del Oro, S. A., we agree to the following: GIVEN THAT: 1. The Area de Conservación Guanacaste (ACG) is a decentralized institution of the National System of Conservation Areas (SINAC) of the Ministry of the Environment and Energy (MINAE), and has the responsibility of continuing its efforts to conserve the biodiversity and ecosystems of its lands into perpetuity.,

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2.

The Fundacion de Parques Nacionales (FPN) functions as a non-profit insitution with the legal capacity to manage funds, including those of the ACG. 3. At the present time the lowland tropical Costa Rican forests that represent the transition between the dry forests of Guanacaste and the Caribbean rainforests are almost totally extinguished, and very poorly represented in Costa Rica’s conserved wildlands, including the ACG, 4. Approximately 1200 ha of the dry-wet transition forests mentioned above still exist in the form of wide peninsulas of forest extending into the Del Oro plantations, and these peninsulas of forest are contiguous with the ACG forests at the southern boundary of Del Oro with the northern limit of the ACG, 5. Del Oro recognizes that the ACG offers a variety of biodiversity and ecosystem services (in sum, known as environmental services) to the Del Oro plantations and its juice production industry, 6. Del Oro supports the concept of purchasing these biodiversity and ecosystem services from the ACG, following the schema proposed below, and Del Oro, MINAE (ACG) and the FPN agree to: 1. Segregate the above-mentioned lands of 1200 ha of dry-wet transitional forest and set their value at $400/ha, and pass them permanently to the FPN/ACG, in payment for the services summarized in Article 9 below. The ACG will conduct this topographic segregation with its own topographer and carry out the passing of these lands to the FPN/ACG, and assume the associated costs, which will be paid by the ACG with its own resources. 2. Value the services of biological control agents coming from the ACG forests (primarily parasitic wasps and flies of importance to Integrated Pest Control) at $1/ha per year for the 1685 ha of adjacent Del Oro orange plantations for the 20 years of the contract, for a total of $1,685/year. 3. Value the technical services of the ACG at $500/day for international consultants and $200/day for national consultants. Del Oro will pay for a minimum of 3 days and 10 days, respectively, per year, for the 20 years of this contract, for a minimum of $3,500 of consultant services, irrespective of whether Del Oro uses these services or not. Additional days will be charged at these same rates but are not included within this contract. 4. Value the provision of water to the Del Oro farms at $5/ha/year for the 1169 ha of the drainage basin of the Rio Mena that lies in the ACG, for a total of $5,885/year for the 20 years of this contract. It is understood that other minor water sources draining from the ACG into the Del Oro farms at no cost are not included in this valuation. 5. Value the biodegredation of the orange peels from Del Oro on ACG lands at $11.93/truckload, for a minimum payment of 1000 truckloads per year, whether used or not, for a minimum of $11,930/ year for the 20 years of the contract. The ACG will design a 20 ha Biodiversity Processing Ground (PBG) to the east of Del Oro, at some point in Sector El Hacha to receive the orange peels. Del Oro agrees to visit the site at the end of the deposition period (end of May) and level the peels to generate an approximately flat layer. The ACG will select another 20 adjacent hectares for the peels in the next year, and continue doing this in four year rotation cycles for a given PBG. Del Oro agrees to maintain the access road and its bridges to the PBGs passable at Del Oro’s cost for these 20 years. Del Oro agrees to maintain a registry of the number of truckloads of peel that are deposited at a PBG each year. 6. Value at $1000/year the rent for the use of a hectare of old pasture within the ACG wildlands but far from any orange plantation or other citrus trees, where Del Oro may plant an arboretum of citrus trees free of diseases, from which they can obtain material for grafts. This environmental service to Del Oro is protection from pests via isolation. Del Oro will pay for and continue any maintenance associated with this hectare for protection against any kind of threat. Del Oro agrees to not apply pesticides or other chemicals that are toxic to biodiversity to this hectare without first having written permission from the ACG. The ACG has full authority to deny such permission without affecting this agreement. 7. If the ACG uses these 1200 ha of land in a carbon fixation program during the 20 year duration of the contract, the carbon credits generated will be divided evenly between Del Oro and the ACG. 8. Del Oro will maintain good agricultural practices in its plantations according the standards and legislation of Costa Rica and the US FDA. As long as Del Oro complies with these standards, the ACG will not interfere with Del Oro’s agricultural activities, thereby explictly recognizing the legitimacy of agriculture on Del Oro’s private lands. 9. The biodiversity services and ecosystem services (environmental services) described above in articles 2–6 are worth $1,685 + $3,500 + $5,885 + $11,930 + $1,000 = $24,000/year. The 1200 ha are worth $480,000. This means that the land that the FPN will receive permanently from Del Oro for the ACG/MINAE is worth 20 years of environmental services from the ACG/MINAE, as are described in articles 1–9. This contract applies for 20 years beginning one year before the date of its signing. The passage of the lands from Del Oro to the FPN/ACG will occur within six months after of the signing date. Being in agreement with all said above, we sign in San Jose, 24 August 1998. CARLOS MANUEL RODRIGUEZ ECHANDI MINISTRO A. I. DE MINAE NORMAN JUSTIN BRAITHWAITE GRUPO DEL ORO, S. A. HONOR WITNESS MIGUEL ANGEL RODRIGUEZ PRESIDENTE DE LA REPUBLICA WITNESSES: MICHAEL BAX GRUPO DEL ORO, S. A. SIGIFREDO MARIN ZUNIGA DIRECTOR AREA DE CONSERVACION GUANACASTE more information about the ACG: http://www.acguanacaste.ac.cr .

APPENDIX II (Translated from the Spanish original.) NUMBER NINE HUNDRED NINETY-NINE. Before me, Marco Vinicio Retana Mora, public notary, with an office in San Jose [COSTA RICA], the following people are present: Johnny Enrique Rosales Cordoba, adult, married, agricultural economist, resident of Monteverde, Puntarenas, identity card number 1–484–951, acting as representative of the entity, the Monteverde Conservation League, and Fernando Sanchez Sirias, adult, married, business administrator, resident of San Jose, identity card number 3–230–568, acting as representative of the entity, Inversiones La Manguera Sociedad Anonima, and these parties declare the following: that in fulfillment of the pre-contract signed by these same parties present here, on 11 March 1998 they come to celebrate this Environmental Services Contract, that will be governed by the following clauses: CHAPTER ONE. SUBJECTS: ONE. THE PARTIES: the parties of this contract are: a)- the Monteverde Conservation League, operating license number 3– 002-075864 (which will be known as the “MCL” herein, for the purposes of this contract), and b)- Inversiones La Manguera Sociedad Anonima (which will be known as the “INMAN” herein, for the purposes of this contract). TWO. REPRESENTATION: The MCL is represented here by its Executive Director, with unlimited power of attorney, Mr. Johnny Enrique Rosales Cordoba, adult, married, agricultural economist, resident of Monteverde, Puntarenas, identity card number 1–484–951, representation inscribed in the Register of Associations of the

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Public Register, record 1983, title 136 and following. The INMAN is represented here by the President of the Board of Directors, Mr. Fernando Sanchez Sirias, adult, married, business administrator, resident of San Jose, identity card number 3–230–568, representation inscribed in the Mercantile Section of the Public Register, at volumes 747 and 1078, titles 269 and 150, sites 475 and 152. THREE. CONTRACTUAL DOMICILES: The parties name the following places as their contractual domiciles, for the effects of article four of Law Number 7637 of 4 November 1996: MCL: their offices located in front of the Gasoline Station in Cerro Plano, Monteverde, Puntarenas. INMAN, 9 Avenue, 13 & 15 Streets, Number 1350, Office 7, San Jose. CHAPTER TWO FOUR. OBJECT: The MCL is the founder, promoter and administrator of the private reserve, the “Children’s Eternal Rain Forest” (Bosque Eterno de los Niños), in which a part of the Esperanza River watershed is enclosed; the part owned by the MCL within the larger watershed area is a land extension close to 3800 hectares. And so, the object of this contract will be environmental services that the MCL will offer to the Esperanza Hydro-electric Project (property of INMAN), environmental services that are carried out across its conservation activities within the Children’s Eternal Rain Forest. FIVE. DEFINED AREA OF ACTION. In spite of what was mentioned in the aforementioned fourth clause, the parties have established and accepted that INMAN will receive a direct benefit via environmental services, provided by the MCL, specifically for the protection and conservation of forest, in a land extension of 3000 hectares, and for that, this last extension of land is what is subjected to environmental services stipulated here, that consequently is and always will be the taxable base of rent for environmental services, that is established later on, even and when, by future purchases or donations of land, the extension of the reserve protected by the MCL would be able to be increased. This determination of three thousand hectares, only can be varied by mutual agreement by both parties, in a public document. Both parties renounce judicial complaints and any other type of complaint, to increase or reduce the extension of land subjected to environmental services. SIX. DEFINITION OF ENVIRONMENTAL SERVICES: For the purposes of this contract, environmental services are understood as those goods or services that, in direct or indirect form, are obtained thanks to the existence of an eco-system like that which is natural forest. The benefits derived from the existence of forest are varied: stabilization of land, soil protection, humidity and nutrient retention, water protection, protection of species biodiversity, protection of genetic biodiversity, scenic beauty, regulation of local and regional climate, and mitigation of gases that produce the greenhouse effect, among others. Environmental services, as yet recognized in Costa Rica, through the Forestry Law Number 7575 of 13 February 1996, are the following: carbon fixation (mitigation of greenhouse-effect gases), protection of water, protection of biodiversity, protection of eco-systems and natural beauty. According to its activities and conservation mission, the MCL promises to protect that part of the Esperanza River watershed that is part of its property, according to what has been defined in this clause. This terrain is completely covered by forest, which offers, among other things, the environmental service of retaining and capturing water, which assure the maintenance of the water flow of the Esperanza River throughout the year. The vegetation cover also maintains the quality of water and prevents landslides and soil erosion, particularly in this steeply inclined terrain, which is the subject of environmental services in this contract. To such effect, the MCL commits itself, within the referred area, to the following: i)- to conserve and protect the existing forest, ii)- to watch for and reject land invasion, iii)- to administer the forest and forest guards and iv)-to attain the economic means to fulfill its commitment, in accord to its absolute discretion, according to its statues. SEVEN. RELATING TO THE TAX OR PAYMENT FOR ENVIRONMENTAL SERVICES: the environmental services to which the previous clause referred have a return favor (quid pro quo) charged to the INMAN, and it is precisely the payment of a price or tax, as was defined in the pre-contract and is retaken in this agreement. The offering of environmental services and the payment of the corresponding tax are independent of the granting of the surface right that is established later on; in case the surface right would be extinguished or would not already be usable to the INMAN, for example due to the confusion with that business’s property, the INMAN’s obligation to the MCL, for paying the tax for environmental services established here, would remain invariable, valid and effective, given that the reasons for the existence of this tax are environmental services and the protection that the MCL offers to the part of the watershed that is on its property and the nonaccess and use of land that is indicated further on. EIGHT. QUANTIFYING THE TAX: The price that INMAN will pay to the MCL, always calculated for three thousand hectares, as defined in the aforementioned fifth clause, is the following: a)- DURING THE CURRENT PERIOD OF CONSTRUCTION, that was estimated as approximately one year. The INMAN will pay to the MCL the sum of three dollars, the monetary unit of the United States of America, per hectare, per year, for an annual total of nine thousand dollars. The INMAN has remitted this sum for the period covering 11 March 1998 to 10 March 1999. In case the construction period would exceed this limit, the INMAN will have to pay an additional sum of six hundred fifty dollars per month. This payment will take place on the 11th day of the month before, in the MCL offices located in Barrio San José de La Tigra, San Carlos. b)- DURING THE FIRST YEAR OF PRODUCTION: The INMAN will pay in advance to the MCL eight dollars per hectare, per year, for an annual total of twenty-four thousand dollars. c)- DURING THE SECOND YEAR OF PRODUCTION: The INMAN will pay in advance to the MCL nine dollars per hectare, for an annual total of twenty-seven thousand dollars. d)- DURING THE THIRD and FOURTH YEAR OF PRODUCTION: The INMAN will pay in advance to the MCL, ten dollars per hectare, per year, for an annual total of thirty thousand dollars. e)- BEGINNING FROM THE FIFTH YEAR OF PRODUCTION: The INMAN will pay to the MCL a tax that will be calculated every six months with the following formula: tax in dollars for each six-month period = three thousand hectares multiplied by 10 dollars per hectare [per year], multiplied: i) - by the resulting factor derived from dividing the real six-month period generation (Note #1: the real generation for each six-month period will be established according to the billing for the total sale of energy that INMAN produces during this period), by the projected annual generation of the hydro-electric plant (Note #2: The projected generation, accepted by ICE at the time of signing of this contract and according to the figures of the Hydro-electric Plant feasibility study provided by INMAN is 28.82 GwH [per year]. However, considering the change in the location of the engine room, there is a new projection of production, that in the case of being approved by ICE, would change this number to 31.70 GwH [per year], which would represent a 10% increase.), according to the feasibility study by INMAN and ii)- by the resulting factor derived from dividing the tariff for Kw/h charged by INMAN during the six-month period, by the tariff for Kw/h that ICE should pay to INMAN at the date in which the project should initiate the sale of energy. In case the INMAN will pay with the energy production, whatever service of ICE or of other public or private business, this payment in kind will be included as part of the real generation that the formula indicates. NINE: CALCULATION OF THE TAX: The estimated annual generation and the tariff at the initiation of the production, indicated in the formula, point “e” of the previous clause, will be established as constants, at the moment in which the project should initiate the sale of energy. This information will be incorporated in this contract by means of an addendum. The six-month period generation will be established against the billing for the sale of energy by the INMAN to ICE and/or any other future buyer. The valid tariff during the six-month period will be established against the data offered by ICE, the INMAN or any other buyer. In this act, the INMAN authorizes the MCL to solicit that information from the respective source. These data will be supplied by INMAN to the fiduciary that will be named, with a copy to the MCL. The calculation of the six-month tax, beginning at the time when this formula should be duly applied, will be done by the fiduciary in charge of the payment, according to what is established in clause eleven. When the MCL will require as such, across one of its representatives the INMAN will provide the necessary information to corroborate the calculations made by the fiduciary. TEN. THE TAX IN CASE OF UNPRODUCTIVITY: It is understood that in the case that the hydroelectric plant would suspend its operation, the amount of the tax will be decreased by the same proportion, as is implied in the formula. Nevertheless, during the first four years of production of the plant, in which a fixed tariff is applied, this circumstance of unproductivity of the plant will be taken in to account to diminished the tax, in the following way: The amount of the annual tax will be divided into 365 (days in a year) to obtain the payment factor for each day, and will be multiplied by the days or fraction of day in which the production has been suspended. By that amount the amount of payment tax will be decreased. ELEVEN. FORM OF PAYMENT OF

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THE TAX: In the first four years of production, the payment of the tax will be made one year in advance. Beginning from the fifth year, the payment of the tax will be made payable every six-months. The initial year will be computed beginning from the day in which the hydroelectric plant enters operation. The payment of the tax will be payable on demand, thirty days after the date on which the hydroelectric plant enters operation and thus successively during the first four years. Beginning >from the fifth year, the payment of the tax will be payable thirty days after the expiration of the six-month period which is addressed. The payment of the tax will be made in dollars, the monetary unit of the United States of America or the equivalent amount in colones, determined by the banking exchange rate. The payment will be made across an ad-hoc trust fund that will be established with the Coperacion Privada de Inversiones, with one of its subsidiaries or with a state bank, as fiduciaries, with the exception that unless that another mechanism should be negotiated that is satisfactory to both parties, which necessarily will be made in writing and through an addendum to this contract. From the establishment of the trust fund, the INMAN, in the capacity of the fiduciary’s client, will give the specific and unconditional order to the fiduciary for the calculation and payment of the tax to the Monteverde Conservation League. In all cases, the INMAN remains obliged to communicate to the Costa Rican Institute of Electricity (ICE) or any other business, public or private, that may become a purchaser of its energy, an order so that the amount of the tax will be drawn on this ad-hoc trust fund on the appropriate months, to fulfill the payments established in this contract. The conditions indicated here will be duly incorporated to the resulting ad-hoc trust fund. CHAPTER THREE: LAND CONFLICT ISSUE: TWELVE. RELATING TO THE LAND IN CONFLICT: In addition, between the two parties there exists a land conflict that appears in the overlap of land register plan number A9609431–91 (from the MCL) and number A-7405816–88 (from INMAN). The overlap appears exactly in the place where INMAN needs to construct a dam and water intake structure for the Esperanza River Hydroelectric Project. This overlap has an extension of approximately five thousand five hundred squared meters. THIRTEEN. RELATING TO THE POSITION OF THE PARTIES WITH RESPECT TO THE LAND: Neither of the parties accept any other position except that the land is their own property; nevertheless, both parties have accepted that currently the MCL finds itself in possession of the land described in the previous clause and that it has boundary lines marking the border in accordance to the land register plan number A-9609431–91. Since the past May 11, INMAN has come soliciting and obtaining from the MCL permits for the use of the aforementioned land, to carry out the work described in the construction plans of the Esperanza River Hydro-electric Project (which was attached to the pre-contract), work that began execution this past 16 April. FOURTEEN. JOINT ACTION FOR THE JUDICIAL SOLUTION OVER THE PROPERTY: The parties mutually recognize the right of making use of the pertinent judicial action to clarify the definitive property of the land referred to in the previous clause. In the measurement of what is possible they will attempt to initiate a joint action in this sense. Further, the parties will hire a topographical engineer, with the purpose of registering a plan of the area of overlap. The MCL promises to establish homesteading rights proceedings, with the purpose of obtaining a valid title in the National Registry of Real Estate, of the land described in land register plan number A-9609431–91, and further, to register, on behalf of INMAN the part of this land that corresponds to the surface right that is indicated in the following clause. FIFTEEN. RELATING TO THE SURFACE RIGHT IN FAVOR OF INMAN: The parties recognized that, while there should be no judicial rulings that would establish the contrary, the MCL is the title holder of the domain and it exercises in effective form the right of possession over the overlapping land. In such state, the MCL grants in this act the surface right in favor of INMAN, over the land that has been named as the conflict zone. The surface right consists of the right to build on the land and utilize the land and the infrastructure that may be constructed there, in exclusive and autonomous form, the MCL retaining the rights to any infrastructure built on this land. The work to create infrastructure on this land will be that for the dam and water intake structure for the Esperanza River Hydro-electric Project (in accord with the specification of the plans that were attached to the pre-contract). The term of this surface right is 99 years, counted from today. This term will be deferrable by written agreement from both parties, in public documentation. The INMAN acknowledges to the benefit of the MCL an annual tax as a return favor of the surface right, established here. This annual tax corresponds to one percent of the value of the infrastructure constructed on the land, in such a way that at the end of the term of the surface right, the infrastructure will have been paid-off and will be the exclusive property of the MCL, without the INMAN being able to reclaim any indemnification for improvement to the land, or, moreover, to the co-property for the infrastructure access to the land. The tax established in this clause will not be paid in money or any other denomination, rather only in the paying-off of the infrastructure in favor of the MCL. In case of the prorogation of the surface right, the tax for the use of the dam and water intake structure will be maintained in one percent of the annual value of the infrastructure existing on the land referenced in this clause. This tax will be paid in cash by the INMAN to the MCL one year in advance. The parties, aware that the surface right cannot be registered over the MCL’s property because even that property itself is not registered, promise at this moment to effect the titling of the land in the name of the MCL, in such a way that the registration of the surface right is given together with the registration of the title for the property in question. Due to the surface right being treated as an atypical right in real Costa Rican law, in the case the Registrar or courts were to impose an obstacle to the registration of the surface right, the parties promise to formalize another type of contract, starting with a usufruct contract, that may assure the real rights of use for INMAN over the land where the structure for the dam and water intake of the hydro-electric project is located, until completing the same aforementioned 99 years for the surface right and under the same conditions or that the contract may not be more onerous for the INMAN. In any case, it is agreed that the surface right remains contingent on the payment of the tax for environmental services for the protection of the hydro-electric watershed, established in the contract. The surface right or eventual usufruct right is subject to the resolution condition in such a way that the INMAN will be left to carry out at least one of the tax payments for environmental services within one month following its liability, the surface right will be dissolved and the MCL will recover the full domain of the land, together with the infrastructure by way of the damages and losses for the nonfulfillment of the contract. On the other hand, it is established that the surface right will be extinguished for the following reasons: a)- The enactment of the resolution condition for non-fulfillment of the tax payment for environmental services, in accord with what is established in clauses seven, eight, nine, ten, eleven and sixteen, although it may be reiterated here that the nature of that tax is like a return favor for the environmental services, not as a return favor for the surface right that is constituted here. b)-Confusion, in case it would come to be determined, judicially or extra-judicially, that the land in dispute is the property of the INMAN, and c)- the expiration of the term. Finally, the land over which the surface right is located is graphically represented in the attached plan, which the parties sign and incorporate as a document to this contract. SIXTEEN. DETERMINATION OF NON-FULFILLMENT OF THE PAYMENT OF THE TAX. Just as it is indicated in the precontract, the figure established here will be utilized to objectively determine an eventual non-fulfillment of the payment of the tax by the INMAN. In case there may be differences to what is agreed here, the INMAN and the MCL accept that they will be resolved by means of arbitration, conforming to the Rule of Arbitration of the Center of Reconciliation and Arbitration of the Chamber of Commerce of Costa Rica, to whose norms the parties will submit unconditionally. The procedure will be the following: when the MCL should consider that the INMAN has defaulted on the tax payment, it will solicit action from the Center of Reconciliation, so that they may become aware of the case. The INMAN will have to present its defense within 15 working days following notification and, further, it will have to pay-off half of the fees corresponding to the Center of Reconciliation’s action, in the adverse case, it will not listen to its defense. In principle the

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expense incurred for the hiring of the Center of Reconciliation will be paid equally by both parties, the MCL and the INMAN. The MCL will pay its half when it presents its motion for action. In the case that it should be determined that indeed there was default on the payment of the tax, the INMAN will have to reimburse the MCL the money it paid to the Center of Reconciliation. If it should be determined that there was no default on the payment of the tax, the INMAN will be able to deduct from the tax for environmental services that which it paid to the Center of Reconciliation. In any case, if the Center of Reconciliation establishes that there was a default on the tax payment, the resolution condition will apply and the surface right will be extinguished. The MCL will keep the improvements to the land, by way of damages and losses, being absolved from covering any amount for them. SEVENTEEN. RELATING TO THE USE OF THE MCL NAME: As part of this agreement, it is established that it is prohibited for the INMAN to make use of the name of the MCL or the Children’s Eternal Rain Forest (Bosque Eterno de los Niños), without prior, written authorization. This is all. The following people serve as honorary witnesses to the signing of the contract: Joyce Mary Zurcher Blen, adult, married, Doctorate of Philosophy, resident of Alajuela, who carries identity card number 1–286–801, ExOmbudsman of the People; Francis John Joyce Hammil, adult, married, biologist, resident of Monteverde, Puntarenas, USA citizen with passport number Z7047463, as President of the Board of Directors of the MCL; Miguel Ruperto Cifuentes Arias, adult, married, biologist, resident of Turrialba, Cartago, citizen of Ecuador with international mission identity card number 4231, as the Central American regional representative of the World Wide Fund for Nature (World Wildlife Fund); and Martha Eugenia Marin Malandez, adult, single, biologist, resident of Sabanilla de Montes de Oca, who carries identity card number 1–584–656, as the Executive Director of the Costa Rican Network of Nature Reserves. I issue the two first testimonies. The aforementioned read to the parties, it is in agreement to them, they approve it and we all sign it in San Jose [COSTA RICA], at sixteen hundred hours on the 28th of October 1998. 1. Janzen, D. H. (1997) in Biodiversity and Human Health, eds. Grifo, F. & Rosenthal, J. (Island Press , Washington, DC), pp. 302–311 . 2. Janzen, D. H. (1998) Science 279, 1312–1313 . 3. Janzen, D. H. (1984) Crafoord Lectures (Royal Swedish Academy of Sciences , Stockholm, Sweden), pp. 2–20 . 4. Orians, G. H. (1998) Bull. Ecol. Soc. Am. 79, 15–28 . 5. Janzen, D. H. & Gómez, R. (1997) in Biodiversity Information: Needs and Options, eds. Hawksworth, D. L. , Kirk, P. M. & Dextre Clarke, S. (CAB International , Wallingford, U.K.), pp. 21–29 . 6. Reid, W. V. , Laird, S. A. , Gómez, R. , Sittenfeld, A. , Janzen, D. H. , Gollin, M. A. & Juma, C. , eds. (1993) Biodiversity Prospecting (World Resources Institute , Washington, DC). 7. Makhubu, L. (1998) Science 282, 41–42 . 8. Janzen, D. H. (1998) Env. Forum 15 , 40 . 9. Janzen, D. H. (1998) in Nature and Human Society: The Quest for a Sustainable World, eds. Raven, P. & Williams, T. (Natl. Acad. Press , Washington, DC), in press . 10. Daily, G. C. (1997) Nature’s Services: Societal Dependence on Natural Ecosystems (Island Press , Washington, DC). 11. Tilman, D. (1998) Nature (London) 396, 211–212 . 12. Livernash, R. , ed. (1998) Valuing the Global Environment: Actions and Investments for a 21st Century (Global Environmental Facility , Washington, DC). 13. Janzen, D. H. , Hallwachs, W. , Jimenez, J. & Gómez, R. (1993) in Biodiversity Prospecting, eds. Reid, W. V. , Laird, S. A. , Meyer, C. A. , Gamez, R. , Sittenfeld, A. , Janzen, D. H. , Gollin, M. A. & Juma, C. (World Resources Institute , Washington, DC), pp. 223–254 . 14. Janzen, D. H. (1973) Science 182, 1212–1219 . 15. Bazzaz, F. , Ceballos, G. , Davis, M. , Dirzo, R. , Ehrlich, P. R. , Eisner, T. , Levin, S. , Lawton, J. H. , Lubchenco, J. , Matson, P. A. , et al. (1998) Science 282, 879 .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Global environmental impacts of agricultural expansion: The need for sustainable and efficient practices

DAVID TILMAN Department of Ecology, Evolution, and Behavior, University of Minnesota, 1987 Upper Buford Circle, St. Paul, MN 55108 ABSTRACT The recent intensification of agriculture, and the prospects of future intensification, will have major detrimental impacts on the nonagricultural terrestrial and aquatic ecosystems of the world. The doubling of agricultural food production during the past 35 years was associated with a 6.87-fold increase in nitrogen fertilization, a 3.48-fold increase in phosphorus fertilization, a 1.68-fold increase in the amount of irrigated cropland, and a 1.1-fold increase in land in cultivation. Based on a simple linear extension of past trends, the anticipated next doubling of global food production would be associated with approximately 3-fold increases in nitrogen and phosphorus fertilization rates, a doubling of the irrigated land area, and an 18% increase in cropland. These projected changes would have dramatic impacts on the diversity, composition, and functioning of the remaining natural ecosystems of the world, and on their ability to provide society with a variety of essential ecosystem services. The largest impacts would be on freshwater and marine ecosystems, which would be greatly eutrophied by high rates of nitrogen and phosphorus release from agricultural fields. Aquatic nutrient eutrophication can lead to loss of biodiversity, outbreaks of nuisance species, shifts in the structure of food chains, and impairment of fisheries. Because of aerial redistribution of various forms of nitrogen, agricultural intensification also would eutrophy many natural terrestrial ecosystems and contribute to atmospheric accumulation of greenhouse gases. These detrimental environmental impacts of agriculture can be minimized only if there is much more efficient use and recycling of nitrogen and phosphorus in agroecosystems. The agricultural achievements of the past 35 years have been impressive. Grain production, mainly from wheat, rice, and maize, has increased at a rate greater than human population. This has decreased the number of malnourished people even as the earth’s human population doubled to 5.8 billion. Although the estimates vary widely, world population is projected to increase about 75% before leveling off at about 10 billion. In combination with increasing demand for meat in developing countries and the use of grains as livestock feed, this increased population density should cause world demand for grain production to more than double. This raises several important questions. If it is possible for world food production to double, again, within the next four or five decades, what impacts would this doubling have on the functioning of the nonagricultural ecosystems of the world, and on the services they provide to humanity? What routes might be used to decrease such impacts? I explore these questions first by asking what the global ecological impacts of “more of the same” agriculture might be, and then by considering practices that might decrease such impacts. In particular, insights are sought in the parallels between natural and agricultural ecosystems, but no easy answers are uncovered. Rather, a new long-term, multidisciplinary research program is needed to develop agricultural methods that can feed a growing world and still preserve the vital services provided to humanity by the world’s natural ecosystems. Current agricultural practices involve deliberately maintaining ecosystems in a highly simplified, disturbed, and nutrient-rich state. To maximize crop yields, crop plant varieties are carefully selected to match local growing conditions. Limiting factors, especially water, mineral nitrogen, and mineral phosphate, are supplied in excess, and pests are actively controlled. These three features of modern agriculture—control of crops and their genetics, of soil fertility via chemical fertilization and irrigation, and of pests (weeds, insects, and pathogens) via chemical pesticides—are the hallmarks of the green revolution. They have caused four once-rare plants (barley, maize, rice, and wheat) to become the dominant plants on earth as humans became the dominant animal. Indeed, these four annual grasses now occupy, respectively, 67 million hectares, 140 million hectares, 151 million hectares, and 230 million hectares, each, worldwide, which is 39.8% of global cropland. For comparison, the total forested area of the United States, including Alaska, is 298 million hectares. Entire regions of the world now are dominated by virtual monocultures of a given crop. These monocultures have replaced natural ecosystems that once contained hundreds to even thousands of plant species, thousands of insect species, and many species of vertebrates. Thus, agriculture has caused a significant simplification and homogenization of the world’s ecosystems. It is as difficult to predict the future of agriculture now as it would have been to anticipate, in 1950, the successes and impacts of the green revolution. However, some insights may be provided by an analysis of the broad trends that occurred during the recent doubling of global food production. These trends may give some insight into the global environmental impacts that the anticipated second doubling of agricultural productivity may have. Next, I consider insights that ecology may offer into the sustainability and stability of agricultural ecosystems. Finally, I pose the major environmental challenges that face humanity as global human population and demand for food continues to increase.

THE ECOLOGY OF DOUBLING CROP PRODUCTION The Food and Agriculture Organization (FAO) database (1) provides a wealth of information on agricultural activities for individual nations, regions, and the world from 1961 to the present. Using the FAO data, let’s look at the pattern of world food production during this period and the factors that allowed it to almost double. The majority of the food crops grown on the arable lands of the earth are cereals (barley, maize, rice, and wheat), coarse grains, and root crops. For convenience, I

PNAS is available online at www.pnas.org. Abbreviation: FAO, Food and Agriculture Organization.

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will call the sum of these world food production. In 1996, cereals comprised 57% of this total, coarse grains 25%, and root crops 18%. By using this measure, world food production, as estimated from the FAO database (1), almost doubled (increased 1.97-fold) from 1961 to 1996 (Fig. 1). Comparable patterns, and comparable ecological implications, occur if just cereal production was considered, or if production for just Europe and the United States, for which better data are available, was considered. Many factors contributed to the recent doubling of world food production. The development of higher-yielding strains of crops and better agricultural practices were important, as were increased use of herbicides for weed control and insecticides and fungicides for pest control. In addition, there were marked increases in the amounts of nitrogen and phosphorus fertilizers applied each year worldwide, in the proportion of arable land that was irrigated, and in the total amount of land that was cultivated annually worldwide (Fig. 2). It was the combined effects of all of these factors, and more, that allowed world food production to double in 35 years. The FAO data (1) show that this recent doubling of world food production was accompanied by 6.87- and 3.48-fold increases in the global annual rate of nitrogen and phosphorus fertilization, respectively, by a doubling in the amount of land that was irrigated, and by a 10% increase in the amount of land in cultivation (Fig. 2). What might be required to allow food production to double again? A simple, naive and optimistic scenario might assume that, during the next four decades, all of the relationships of Fig. 2 would remain linear and gains in crop genetics, weed and pest control, and cultivation practices would continue at their previous pace. The assumption of linearity can be used to predict the rates of nitrogen and phosphorus fertilization and irrigation, and the increase in amount of cultivated land needed to double food production. Even this scenario, though, would require, based on the linear regression of Fig. 2A , that the global rate of application of nitrogen fertilizer increase from about 75 × 106 metric tons per year to 235 × 106 metric tons per year. Nitrogen fixed by legume crops also would need to more than triple. Comparable calculations, based on the regression of Fig. 2B , predict that the global annual rate of application of phosphorus fertilizer would have to increase from about 37 × 106 metric tons per year to 94 × 106 metric tons per year for food production to double. Similarly, the worldwide proportion of arable lands that are irrigated would have to increase from the current 17% to about 32% (based on extrapolation of Fig. 2C), and the total amount of land in cultivation would have to increase from about 1.47 × 109 hectares to 1.73 × 109 hectares (extrapolation of Fig. 2D). These changes represent a worldwide tripling of the annual rates of N and P fertilization, a doubling of the extent of irrigation, and an 18% increase in the amount of land farmed.

FIG. 1. Based on FAO data (1), world food production, measured as the sum of cereals, coarse grains and root crops, almost doubled from 1961 to 1996. A linear regression, and 95% and 99% confidence intervals for the regression, are shown.

FIG. 2. The relationship between annual global food production (cereals + coarse grains + root crops) and agricultural inputs, based on FAO data (1). (A) Global annual nitrogen fertilization rate. (B) Global annual phosphorus fertilization rate. (C) Proportion of arable lands that are irrigated. (D) Total land surface in agricultural crop production. Such linear projections of yields may be overly optimistic for a variety of reasons. First, the yield of a crop is a saturating

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function of the rate of supply of its limiting resource. Adding fertilizer to already well-fertilized areas, such as productive croplands in the developed nations that produce the majority of the world’s cereals, will have little impact on yield. Significant regional gains, though, can be achieved in many developing countries by appropriately fertilizing croplands not currently receiving fertilizer. Similar saturating yield curves occur for phosphorus and irrigation. In total, such saturating curves imply that it may be difficult to increase yields at a pace similar to that of the past four decades. Second, the easiest and greatest gains from crop breeding programs may have already occurred (2). Annual gains in yields from breeding programs are decreasing, and the research costs associated with these gains are escalating (2). This is not surprising. Given a fixed gene pool, the responses to a given selective regime are most rapid initially and increasingly slower through time. Such yield gains represent genetic movement on the morphological and physiology tradeoff surface on which plant species have differentiated and evolved. The closer a given variety is to the optimum point on this tradeoff surface, the less will be the gain from further selection. Once most of the original genetic variance preserved within crop landraces and remaining wild relatives has been exploited, future breeding-based yield gains are likely to be small or difficult to obtain. Marked yield gains from crop breeding then would require that plants overcome major morphological and physiological constraints that no organisms have overcome during hundreds of millions of years of evolution. Organisms that greatly overcame such barriers, perhaps through gene transfers, would be supercompetitive species that could potentially invade into and change the structure of nonagricultural ecosystems (3). These concerns lead me to wonder if global food production can be doubled by a continuation of past practices. The other route for a major increase in food production is a marked increase in arable land, which the FAO data suggest has played a modest role in the past 30 years. Because the best land already has been cultivated, the amount of land dedicated to agriculture may have to increase disproportionately to the gain in global food production.

ECOLOGICAL IMPACTS OF DOUBLING GLOBAL FOOD PRODUCTION If these simple extrapolations of past practices are any indication, doubling global food production will triple the annual rates of nitrogen and phosphorus release to the globe. Current rates of agricultural nitrogen production, via both production of fertilizer and cultivation of legume crops, already approximately equal the natural (preindustrial) rate of addition of biologically active nitrogen to the globe (4). Pointsource releases of phosphorus are tightly regulated in developed nations because phosphorus is a major limiting nutrient in aquatic ecosystems and increases in its supply rate harm water quality and aquatic foodweb structure. A tripling of global phosphorus supply rates is likely to adversely impact many aquatic ecosystems, especially those that have significant inputs of eroded agricultural soils or phosphorus-rich wastes from livestock and poultry. Nitrogen is much more motile in soil than phosphorus because soil bacteria can convert ammonia to nitrate and nitrite, which are readily leached from soil (5). Denitrification by bacteria also can convert nitrate into nitrous oxide, a potent greenhouse gas. In addition, ammonia, which is both directly applied as fertilizer and created via bacterial degradation of animal waste and other organic compounds, is highly volatile. It is transported via air and deposited on other ecosystems with precipitation. These numerous modes of transport mean that agricultural nitrogen, less than half of which stays in a field or is harvested with a crop, impacts both terrestrial and aquatic ecosystems as a eutrophier, and impacts global climate because of is role as a greenhouse gas. Indeed, there is a direct and quantitative link between the amounts of nitrogen in the major rivers of the world and the magnitude of agricultural nitrogen inputs to their watersheds (6). The long-term ecological impacts of increased rates of agricultural nitrogen and phosphorus input will depend on the levels to which these nutrients accumulate in various nonagricultural ecosystems. These levels are uncertain because of the complexities of the global biogeochemistry of nitrogen and phosphorus. These nutrients accumulate in a variety of forms in many different sinks (arable soil organic matter, groundwater, freshwater and marine ecosystems and their sediments, nonagricultural ecosystems, atmospheric nitrous oxide) after agricultural application, but the eventual sizes of these pools will depend on biologically and physically driven rates of transfer in and out of these pools (5). For agricultural nitrogen, one critical step will be the rate and location of denitrification, especially complete denitrification to N2. The transport of phosphorus to nonagricultural ecosystems especially will depend on erosion and surface flow. As emphasized by Socolow (7), a scientific effort comparable to that on the global carbon cycle will be needed to understand the impacts on global biogeochemistry of elevated rates of agricultural nitrogen and phosphorus application. Nitrogen and phosphorus are the two most important limiting nutrients of terrestrial, freshwater, and marine ecosystems (3, 8–11). The impacts of elevated levels of a major limiting nutrient are well documented. Nutrient addition causes dominance by a few, often formerly rare plant and animal species, and the loss of species diversity (e.g. refs. 3 , 9 , 12 , 13 , 14 and 15 ). Both effects are approximately proportional to the cumulative magnitude of nutrient addition. High rates of nitrogen deposition caused by intensive, nitrogen-rich agriculture in the Netherlands were a major cause of the conversion of species-rich native heathlands into monoculture grasslands and then forest (16). At high rates of nutrient addition, nuisance plant species often dominate both terrestrial and aquatic ecosystems. For instance, high rates of nitrogen addition cause prairie grasslands to become virtual monocultures of an otherwise extremely rare nonnative agricultural weed (17). Bluegreen algal species, some toxic, often dominate lakes, rivers and streams that receive high rates of P and N loading. Similarly, blooms of toxic red algae and of pathogenic taxa such as Pfisteria occur in nutrient-polluted marine habitats. Anoxic conditions associated with high rates of phosphorus and nitrogen loading cause fish die-offs in both freshwater and marine ecosystems (18). Unless its efficiency is increased, a doubling of irrigation would pose additional environmental problems. Humans already impact a large portion of the terrestrial hydrologic cycle (19). Additional irrigation would divert more water from aquatic ecosystems and impact groundwaters and surface waters via additional leaching of agrochemicals. A conservative estimate, based on the assumption that future yield gains can match those of the past 35 years, is that doubling global food production will require 18% more arable land. Even this 18% increase would require the loss of 268 million hectares of nonagricultural ecosystems worldwide, comparable in size to cultivating all of the currently forested land of the United States. A doubling of food production may require a much greater increase in land dedicated to agriculture. The resulting ecosystem destruction would vastly increase the proportion of the world’s species threatened with extinction. It also would cause a massive release of CO2 from land clearing and tilling (5). Because highdiversity ecosystems generally occur on infertile soils (3, 9, 20), the conversion of less-fertile ecosystems to agriculture would disproportionately impact world biodiversity.

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AGRICULTURE AND THE LOSS OF ECOSYSTEM SERVICES A doubling of global food production would have major impacts on the ability of nonagricultural ecosystems to provide services (21) vital to humanity. Existing nonagricultural ecosystems provide, at no cost, pure, drinkable water. In contrast, the groundwater associated with intensive agricultural ecosystems often contains sufficiently high concentrations of nitrite and nitrates or of pesticides and their residues as to be unfit for human consumption. Expensive treatment is required to make it potable. The biodiversity of nonagroecosystems provides many services to agriculture. For instance, the genetic diversity of both wild relatives of crop plants and unrelated organisms is used to increase yields and to reduce impacts of agricultural pests and pathogens. However, the maintenance of the wild biodiversity needed for future development of crops and medicines occurs mainly in nonagricultural ecosystems, the very ecosystems threatened by agricultural expansion and nutrient release. Agriculture depends on soil fertility, fertility created by the ecosystems destroyed when lands are converted to agriculture. Especially on sandy soils, the best way to regain soil fertility lost because of tilling is to allow re-establishment of the native ecosystems. Many agricultural crops depend on the pollination services provided by insects, birds, or mammals that live in nearby nonagricultural ecosystems (18). Similarly, agricultural crops benefit from biocontrol agents, such as parasitic and predatory insects, birds, and bats, that live in neighboring nonagricultural ecosystems and that decrease outbreaks of agricultural pests. Nonagricultural ecosystems, such as forests on slopes and wetlands, help meter the release of water into streams and rivers, and thus help in flood control. If properly managed, natural ecosystems also can produce a sustainable supply of goods used by society, including timber and fiber, fish, and game. This brief overview of ecosystem services (21) demonstrates that society, and agriculture, depend on many services provided by nonagricultural ecosystems. Although it is difficult to establish economic values for such services (22), it is clear that, when possible, technological substitutes for lost ecosystem services can be extremely expensive. This highlights the need for public policy to consider the short-term and long-term costs of actions that decrease the ability of nonagricultural ecosystems to provide vital ecosystem services to society.

MORE OF THE SAME WILL NOT WORK The global agricultural enterprise is passing a threshold. It has gone from being a minor source of off-site environmental degradation 35 years ago to becoming the major source of nitrogen and phosphorus loading to terrestrial, freshwater, and marine ecosystems. If this loading increases as projected here, agriculture will adversely transform most of the remaining natural, nonagricultural ecosystems of the world. Because the global environmental impact of agriculture on natural ecosystems and the services they provide may be as serious a problem as global climate change, the impacts of agriculture merit more study. A “more of the same” approach to the doubling of agricultural production will have significant environmental costs, costs that could be lowered by processes that increase the efficiency of fertilizer use, such as precision agriculture (23) and by incentives for their use. Methods that increase the nutrient efficiency of the overall agricultural production process also are needed. For instance, wastes from large-scale animal operations are rich in N and P. Unless properly recycled into arable fields, or subjected to tertiary sewage treatment to remove nitrogen and phosphorus, such wastes can be a major source of N and P loading to nonagricultural ecosystems (24). However, the regulations that apply to municipal sewage and factory effluents often have not been applied to large-scale livestock factories or to heavily fertilized fields, even though these are now major sources of nutrient loading to many aquatic ecosystems (18). The development of more nutrient-efficient crops also could have major environmental benefits. If crops could be bred to consume a larger proportion of soil nitrate and ammonium, this would decrease the amount of unconsumed soil nitrate and ammonium that would be lost via leaching and volatilization. This would decrease impacts on offsite ecosystems. Breeding programs that increased crop yields would decrease some of the future impacts of agriculture by decreasing the amount of additional land that would have to be brought into agricultural production. The ecosystems of the world now are dominated by humans (25). The implications of human domination, including impacts from expanding agricultural activities, must be better understood and incorporated into policy. This will require an on-going, iterative process in which science and policy regulating agricultural practices advance hand-in-hand, much as is being done for the climate issue by the Intergovernmental Panel on Climate Change. This will require predictive, mechanistic models of the impacts of agriculture on nonagricultural ecosystems.

ECOLOGICAL INSIGHTS INTO AGRICULTURAL IMPACTS AND SUSTAINABILITY What might be done to decrease the environmental impacts of agriculture while maintaining or improving its productivity, stability, or sustainability? This major challenge will have no single, easy solution. Partial answers will come from increases in the precision and efficiency of nutrient and pesticide use, from advances in crop genetics including advances from biotechnology, and from a variety of engineering solutions. Some additional insights may come from a consideration of the principles that govern the functioning of all ecosystems, including agroecosystems. Ecosystem functioning is known to depend on the traits of the species ecosystem’s contain (their composition), the number of species they contain (their species diversity), and the physical conditions they experience, especially disturbance regimes. A consideration of the principles governing the impacts of composition, diversity, and disturbance on ecosystems may suggest ways to decrease impacts of agriculture or to make it more productive, stable, or sustainable. It is critical to realize that these principles apply within a given ecosystem type. They describe differences in functioning of otherwise identical ecosystems that share the same species pool and differ only in which and how many species they contain. These principles were not derived from, and do not apply to, comparisons among different ecosystem types, such as cattail swamps versus prairies, or mangrove versus upland forest, or tropical versus temperate forests. A fundamental principle of epidemiology and ecology is that the severity and extent of a disease or pest outbreak depends on the density of the host population. At low host population densities, there is a low chance of contagious spread. However, at high host densities, a disease or pest can spread epidemically throughout the population. An unavoidable effect of high diversity is that most species have lower densities than in low diversity communities. For instance, on average a species is about one-fourth as abundant in a four-species community as in monoculture. This simple effect caused a variety of plant leaf fungal diseases to have lower rates of occurrence at higher plant diversity in a field experiment. Agriculture has transformed once-rare plants into some of the most abundant species on earth. Maize, which once occurred in scattered multispecies mixtures on nutrient-poor or disturbed soils, now covers 140 million hectares of the earth. Potential pathogens and pests that never had encountered maize now do so frequently. Pests and pathogens that formerly could not have maintained populations on maize now encoun-

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ter hosts growing at much greater local and regional densities and with higher tissue nutritional levels. Just as humans have accumulated diseases as densities increased during the past 2,000 years (26), so, too, will major crops continue to accumulate diseases and pests. Southern corn blight is one such disease. A strain of western corn rootworm that is newly adapted to living on both corn and soybeans is an emerging pest. Wheat head rust is another disease. The latter virtually eliminated wheat as a major rotation crop from Indiana and Illinois in the 1920s and now is doing so in western Minnesota and eastern North and South Dakota. Plant diseases and pests can have devastating impacts. The American chestnut, once a dominant tree of eastern U.S. forests, and the American elm both were virtually eliminated after pathogens, to which no known resistance occurs, invaded North America. Similarly, novel pests or pathogens or strains of pathogens could either greatly reduce the area in which wheat, rice, or maize can be grown or, perhaps, eliminate these as viable crops. A major protection against these possibilities is diversity—the diversity of crops deployed in a region, the diversity of substitute crops, and the diversity of genetic resistances within crops. All else being equal, the stability of the total rate of plant production in an ecosystem depends on both the species diversity of the plant community and its species composition (e.g. refs. 15 and 27 , 28 , 29 ). The stability of primary productivity is greater for ecosystems containing greater plant diversity (15, 28). This results from three underlying processes. First, the same statistical averaging process that causes more diverse portfolios of stocks to be more stable than less diverse portfolios applies to ecosystems (30–32). Second, interspecific competition causes negative covariances in the abundances of species, and such compensatory effects can act to more greatly stabilize more diverse ecosystems (15, 32). Third, the increase in ecosystem productivity that occurs as diversity increases, termed overyielding, also tends to stabilize primary productivity at higher diversity (32). The greater stability of more diverse ecosystems means that diversity has an insurance value by minimizing year-to-year variance in yields. Greater stability of agricultural yields might be attained by growing, as a single crop, a mixture of appropriately chosen genotypes of a given species, such as a mixture of high-yielding hybrid varieties. The plant species diversity of an ecosystem, and its plant species composition, influence its primary productivity (33– 38). Total primary productivity increases about 35–70% as plant species diversity increases from one to about 20 species. Such effects have a series of alternative theoretical explanations (27, 32, 39–41). The two major classes of explanations are the sampling effect and niche differentiation. The sampling effect implies that the increase in productivity associated with greater plant diversity is caused by the higher probability that a more productive species or variety will be present in a more diverse plot. The niche differentiation effect is based on complementary use of different limiting resources by different species. One strain or species may grow best during the cooler portion of the growing season, and another during the warmer portion. Or one may better exploit soil nutrients in deeper soils and another at shallower depths. Such differing abilities to use limiting resources cause productivity to increase with diversity (41). Under conditions typical of high-intensity agriculture (fertilized, irrigated fields in which light limits the growth of all plants), the sampling effect theory should apply, with maximal yields provided by the appropriate monoculture. All major grain crops (corn, wheat, rice, barley, etc.), soybeans, sugar cane, and most other crops are grown in monoculture. However hay, some crops harvested for fodder, and grasslands maintained for grazing often are grown under conditions in which niche differences could allow benefits from diversity. Crop diversity also may be of benefit when arable lands are managed to optimize yield in the face of constraints on nutrient release to the environment. Recent theory has predicted (35) and recent field experiments have shown (36, 37) that the rates of loss of limiting nutrients from terrestrial ecosystems are lower at higher plant diversity, and are equally impacted by species composition. Cultivation has major effects on soil fertility. Within the first 50 years of tilling, 40–70% of the original store of soil organic matter (carbon and nitrogen) is lost (42). For porous sandy soils, which start with relatively low organic matter and nitrogen, the loss of fertility during farming can be so great that the soils cannot be sustainably farmed. Recovery of soil C and N should be more rapid if abandoned fields are planted with a high-diversity mixture of appropriate plant species. On the sandy soils of my research site in central Minnesota, native warm-season prairie grasses and legumes, combined, significantly increase the rate of recovery of soil fertility after agriculture (43). Programs designed to restore soil fertility, such as land set-aside programs, may be more successful if such lands are planted to high-diversity mixtures of appropriate species. Finally, in higher diversity ecosystems, there is more complete use of limiting resources (36, 37, 41). The resulting lower concentrations of unconsumed soil nutrients decreases the number of other species that invade an ecosystem (32). Weeds are a major pest of agriculture. In North America, most weedy species are non-native annuals introduced from Europe or Asia. The ability of newly introduced weeds to spread across a landscape will depend on the spatial pattern of agricultural and native high-diversity ecosystems. Landscapes with an appropriate balance of agricultural and natural ecosystems may be more resistant to invasion by new weedy species.

CONCLUSIONS A hallmark of modern agriculture is its use of monocultures grown on fertilized soils. Ecological principles suggest that such monocultures will be relatively unstable, will have high leaching loss of nutrients, will be susceptible to invasion by weedy species, and will have high incidences of diseases and pests—all of which do occur. Although ecological principles may predict these problems, they do not seem to offer any easy solutions to them. Agriculture, and society, seem to be facing tough tradeoffs. Agricultural ecosystems have become incredibly good at producing food, but these increased yields have environmental costs that cannot be ignored, especially if the rates of nitrogen and phosphorus fertilization triple and the amount of land irrigated doubles. The tradition in agriculture has been to maximize production and minimize the cost of food with little regard to impacts on the environment and the services it provides to society. As the world enters an era in which global food production is likely to double, it is critical that agricultural practices be modified to minimize environmental impacts even though many such practices are likely to increase the costs of production. 1. Food and Agriculture Organization (1997) FAOSTAT (Food and Agriculture Organization of the United Nations , Rome). 2. Ruttan, V. W. (1999) Proc. Natl. Acad. Sci. USA 96, 5960–5967 . 3. Tilman, D. (1982) Resource Competition and Community Structure: Monographs in Population Biology (Princeton Univ. Press , Princeton). 4. Vitousek, P. M. , Aber, J. D. , Howarth, R. W. , Likens, G. E. , Matson, P. A. , Schindler, D. W. , Schlesinger, W. H. & Tilman, D. (1997) Ecol. Appl. 7, 737–750 . 5. Schlesinger, W. H. (1991) Biogeochemistry: An Analysis of Global Change (Academic , San Diego). 6. Howarth, R. W. , Billen, G. , Swaney, D. , Townsend, A. , Jaworski, N. , Lajtha, K. , Downing, J. A. , Elmgren, R. , Caraco, N. , Jordan, T. , et al. (1996) Biogeochemistry 35, 181–226 .

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7. Socolow, R. H. (1999) Proc. Natl. Acad. Sci. USA 96, 6001–6008 . 8. Vitousek, P. M. (1984) Ecology 65, 285–298 . 9. Tilman, D. (1980) Am. Nat. 116, 362–393 . 10. Tilman, D. , Kilham, S. S. & Kilham, P. (1982) Annu. Rev. Ecol. System. 13, 349–372 . 11. Smith, V. H. , Tilman, G. D. & Nekola, J. C. (1999) Environ. Pollution, in press . 12. Lawes, J. & Gilbert, J. (1880) Philos. Trans. R. Soc. 171, 289–416 . 13. Thurston, J. (1969) in Ecological Aspects of the Mineral Nutrition of Plants, ed. Rorison, I.(Blackwell Scientific , Oxford) , pp. 3–10 . 14. Patrick, R. (1963) Ann. N.Y. Acad. Sci. 108, 359–365 . 15. Tilman, D. (1996) Ecology 77, 350–363 . 16. Aerts, R. & Berendse, F. (1988) Vegetatio 76, 63–69 . 17. Tilman, D. (1987) Ecol. Monogr. 57, 189–214 . 18. Carpenter, S. R. , Caraco, N. F. , Correll, D. L. , Howarth, R. W. , Sharpley, A. N. & Smith, V. H. (1998) Ecol. Appl. 8, 559–568 . 19. Postel, S. L. , Daily, G. C. & Ehrlich, P. R. (1996) Science 271, 785–788 . 20. Huston, M. A. (1979) Am. Nat. 113, 81–101 . 21. Daily, G. C. (1997) Nature’s Services: Societal Dependence on Natural Ecosystems (Island, Washington, DC). 22. Costanza, R. , d’Arge, R. , de Groot, R. , Farber, S. , Grasso, M. , Hannon, B. , Limburg, K. , Naeem, S. , O’Neill, R. V. , Paruelo, J. , et al. (1997) Nature (London) 387, 253–260 . 23. Matson, P. A. , Parton, W. J. , Power, A. G. & Swift, M. J. (1997) Science 277, 504–509 . 24. Drinkwater, L. E. , Wagoner, P. & Sarrantonio, M. (1998) Nature (London) 396, 262–265 . 25. Vitousek, P. M. , Mooney, H. A. , Lubchenco, J. & Melillo, J. M. (1997) Science 277, 494–499 . 26. Crosby, A. W. (1986) Ecological Imperialism: The Biological Expansion of Europe 900–1900 (Cambridge Univ. Press , Cambridge). 27. McNaughton, S. J. (1993) in Biodiversity and Ecosystem Function, eds., Schulze, E.-D. & Mooney, H. A. (Springer , Berlin) , pp. 361–383 . 28. Tilman, D. & Downing, J. A. (1994) Nature (London) 367, 363–365 . 29. Naeem, S. & Li, S. (1997) Nature (London) 390, 507–509 . 30. Doak, D. F. , Bigger, D. , Harding, E. K. , Marvier, M. A. , O’Malley, R. E. & Thomson, D. (1998) Am. Nat. 151, 264–276 . 31. Tilman, D. , Lehman, C. L. & Bristow, C. E. (1998) Am. Nat. 151, 277–282 . 32. Tilman, D. (1999) Ecology, in press . 33. Naeem, S. , Thompson, L. J. , Lawler, S. P. , Lawton, J. H. & Woodfin, R. M. (1994) Nature (London) 368, 734–737 . 34. Naeem, S. , Thompson, L. J. , Lawler, S. P. , Lawton, J. H. & Woodfin, R. M. (1995) Philos. Trans. R. Soc. London Ser. B 347, 249–262 . 35. Naeem, S. , Håkenson, K. , Lawton, J. H. , Crawley, M. J. & Thompson, L. J. (1996) Oikos 76, 259–264 . 36. Tilman, D. , Wedin, D. & Knops, J. (1996) Nature (London) 379, 718–720 . 37. Tilman, D. , Knops, J. , Wedin, D. , Reich, P. , Ritchie, M. & Siemann, E. (1997) Science 277, 1300–1302 . 38. Symstad, A. J. , Tilman, D. , Willson, J. & Knops, J. M. H. (1998) Oikos 81, 389–397 . 39. Swift, M. J. & Anderson, J. M. (1993) in Biodiversity and Ecosystem Function, eds. Schulze, E.-D. & Mooney, H. A. (Springer , Berlin) , pp. 15–41 . 40. Huston, M. A. (1997) Oecologia 110, 449–460 . 41. Tilman, D. , Lehman, C. L. & Thomson, K. T. (1997) Proc. Natl. Acad. Sci. USA 94, 1857–1861 . 42. Parton, W. J. & Rasmussen, P. E. (1994) Soil Sci. Soc. Am. J. 58, 530–536 . 43. Knops, J. M. H. & Tilman, D. (1999) Ecology, in press .

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This paper was presented at the National Academy of Sciences colloquium “Plants and Population: Is There Time?” held December 5– 6, 1998, at the Arnold and Mabel Beckman Center in Irvine, CA.

Nitrogen management and the future of food: Lessons from the management of energy and carbon

ROBERT H. SOCOLOW * Center for Energy and Environmental Studies, Princeton University, Princeton, NJ 08544 ABSTRACT The food system dominates anthropogenic disruption of the nitrogen cycle by generating excess fixed nitrogen. Excess fixed nitrogen, in various guises, augments the greenhouse effect, diminishes stratospheric ozone, promotes smog, contaminates drinking water, acidifies rain, eutrophies bays and estuaries, and stresses ecosystems. Yet, to date, regulatory efforts to limit these disruptions largely ignore the food system. There are many parallels between food and energy. Food is to nitrogen as energy is to carbon. Nitrogen fertilizer is analogous to fossil fuel. Organic agriculture and agricultural biotechnology play roles analogous to renewable energy and nuclear power in political discourse. Nutrition research resembles energy end-use analysis. Meat is the electricity of food. As the agriculture and food system evolves to contain its impacts on the nitrogen cycle, several lessons can be extracted from energy and carbon: (i) set the goal of ecosystem stabilization; (ii) search the entire production and consumption system (grain, livestock, food distribution, and diet) for opportunities to improve efficiency; (iii) implement cap-and-trade systems for fixed nitrogen; (iv) expand research at the intersection of agriculture and ecology, and (v) focus on the food choices of the prosperous. There are important nitrogen-carbon links. The global increase in fixed nitrogen may be fertilizing the Earth, transferring significant amounts of carbon from the atmosphere to the biosphere, and mitigating global warming. A modern biofuels industry someday may produce biofuels from crop residues or dedicated energy crops, reducing the rate of fossil fuel use, while losses of nitrogen and other nutrients are minimized. The agriculture and food system disrupts the biogeochemical nitrogen cycle at various spatial scales. Limiting the impact of the agriculture and food system on the nitrogen cycle is increasingly important, as that system grows to feed a larger and more affluent world population. Managing the food-nitrogen connection is likely to resemble managing the energy-carbon connection, a task that already has begun. The parallels between food and energy are myriad. In both the food and energy systems, alarms regarding a crisis of global supply were sounded in the 1970s, innovations and adaptations followed that permitted growth to continue, and the focus now is on addressing adverse impacts of further expansions of supply. Problems of scarcity share the stage with problems of abundance. This paper reviews the nitrogen cycle, its disruptions by human activity, and some of the adverse environmental consequences of these disruptions. It then suggests principles, extracted from the energy-and-carbon arena, that might guide modification of the agriculture and food system to increase its responsiveness to nitrogen management objectives.

HOW THE NITROGEN CYCLE WORKS AND HOW IT IS BEING DISRUPTED The Nitrogen Cycle. Given that extensive introductions to the biogeochemical nitrogen cycle are found elsewhere (1–5), a quick tour here may suffice. Nitrogen is found in three forms. It is bound to itself in a two-atom molecule, dinitrogen, or N2; this form is the most abundant, but it is almost unavailable to life because it is so stable that only a few specialized bacteria (and lightning) can break it apart. Nitrogen is bound to carbon, as organic nitrogen, in a magnificent variety of organic molecules, critical to life and present long after death, including proteins and their component amino acids. And it is bound neither to itself nor to carbon, in nitrogen nutrients. Nitrogen nutrients are relatively small molecules, both nitrogen ions and nitrogen gases. The principal nitrogen ions are ammonium (NH4+) and nitrate (NO3−). The nitrogen gases include ammonia (NH3); various oxides of nitrogen, including nitric oxide (NO), nitrogen dioxide (NO2), dinitrogen pentoxide (N2O5), and nitrous oxide (N2O); and nitric acid vapor (HNO3). A specialized vocabulary describes the transformations from one form to another. Fixation is the process of making N2 into nitrogen nutrients (largely NH4+), and denitrification (in effect, unfixing) is the process of rebuilding N2 from nitrogen nutrients (largely NO3−). Nitrification oxidizes ammonium to nitrate. (A complication: Side reactions of both nitrification and denitrification produce N2O.) Assimilation and immobilization are the processes by which nutrients become organic nitrogen (plants assimilate, microorganisms immobilize), and mineralization is the process by which organic nitrogen is decomposed back into nitrogen nutrients. Assimilation, immobilization, and mineralization are capabilities found widely in nature, but fixation and denitrification can be accomplished only by specialized microorganisms. Both air routes and water routes connect nutrient systems across large distances. Denitrification, mineralization, and nitrification all produce nitrogen gases. Once volatilized into the atmosphere, these gases undergo further chemical transformations before returning to the Earth’s surface by wet or dry deposition. Alternatively, nitrogen nutrients and organic nitrogen can be leached into groundwater or carried in runoff into surface water, then transported down waterways in solution or attached to solid particles. The nitrogen cycle is captured quantitatively by the magnitudes of the stocks of nitrogen in the various biological and geophysical “reservoirs” [measured in millions of metric tons of nitrogen, Mt(N), for example] and the flows of nitrogen between pairs of reservoirs (in Mt (N)/yr). The stock of N2 in the atmosphere is so large, 3.9 × 1015 Mt(N), as to be

*To

whom reprint requests should be addressed. e-mail: [email protected] . PNAS is available online at www.pnas.org.

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effectively infinite. The stock of terrestrial organic nitrogen is about 100,000 Mt(N); very little terrestrial fixed nitrogen is in the form of nutrient, because uptake by plants is rapid. Only 4% of the 100,000 Mt(N) of terrestrial organic nitrogen is in living organisms, and the rest is in dead organic matter (5). Of the terrestrial dead organic matter, roughly 15% is labile, and 85% is recalcitrant, the distinction referring to the ease of mineralization. The stock of fixed nitrogen in the ocean, about half nutrients and about half dead organic matter, is roughly 10 times larger than the stock of terrestrial fixed nitrogen (5, 6). Evidence for Human Impact on a Global Scale. The concentration of nitrous oxide in the atmosphere gives indirect information about human impacts on the nitrogen cycle. Records from ice cores reveal that the concentration of nitrous oxide fluctuated only a few percent in the period from 2,000 years ago until about a century ago, when a statistically significant upward climb began. The current concentration, about 310 parts per billion by volume (ppbv), is about 10% higher than the average value before this century, and the current rate of increase is about 0.8 ppbv per year, or 0.3% per year, corresponding to a flow of 4 Mt(N)/yr (5). The stable concentration in earlier times and the rising concentration in the past century are presumed to be evidence that a stable dynamic equilibrium governed the flows of nitrogen among soils, waterways, oceans, and the atmosphere until human activity was boisterous enough to create a detectable signal. A similar story is told by the ice-core record of the atmospheric concentration of carbon dioxide (CO2): the concentration started its upward climb 200 years ago, is currently climbing 0.5% per year, and is now about 30% above its earlier average value. The earlier period of dynamic equilibrium and nearly constant atmospheric concentration is called the preindustrial period; its features are crude averages over several centuries of data, ending roughly in 1800. Specifically, for the preindustrial global nitrogen cycle to have been in dynamic equilibrium requires a constant flow of fixed nitrogen (i) through the fixed-nitrogen subcycle, where nutrient is transformed into organic nitrogen and back (through a loop of assimilation, death, and mineralization); and (ii) through the fixing-unfixing subcycle, where N2 is transformed into nutrient and back. Quantitatively, and restricting attention to the terrestrial component of these subcycles, 1,200 Mt(N)/yr flowed through the fixed nitrogen cycle and 140 Mt(N)/yr flowed through the fixing-unfixing subcycle. Ocean and land nitrogen cycles are linked by river runoff, and coastal zones are active regions of nitrogen transformation. Ocean and land nitrogen cycles also are linked by atmospheric transport of nitrogen gases between land and sea. The flows that form the ocean components of the global nitrogen cycle are poorly known (5). The rate at which nitrogen is being fixed on land today is approximately 300 Mt(N)/yr, roughly double its preindustrial value. Thus, the incremental fixation today from the global industrial and agricultural system of human beings is roughly equal to natural fixation in preindustrial times. This startling result captures the essence of the human impact on the nitrogen cycle. Its consequences depend strongly on the extent to which denitrification has kept pace with fixation. Unfortunately, a quantitative understanding of denitrification rates in various managed and unmanaged terrestrial and aquatic environments is largely missing, probably the biggest obstacle thwarting accurate modeling of the present-day nitrogen cycle (3). Anthropogenic Additions of Fixed Nitrogen. The additional flow of approximately 160 Mt(N)/yr from human nitrogen-fixation activity has three principal components. The two largest are directly related to agriculture: the synthesis of ammonia, largely for nitrogen fertilizer, and land use that enhances biological fixation. Ammonia synthesis is accurately known to be contributing about 95 Mt(N)/yr globally, of which 80 Mt(N)/yr is incorporated into synthetic nitrogen fertilizer, and the rest is “consumed by chemical industries and lost during processing and transportation” (7). The third contributor is high-temperature combustion, estimated, also very roughly, at 30 Mt(N)/yr (8, 9). I examine each of these three in turn. Fertilizer. Nitrogen fertilizer is made from ammonia, and ammonia is made, in effect, fixed, from nitrogen in the air. An ammonia factory requires very high pressures and moderately high temperatures to accomplish what bacteria accomplish at ordinary pressures and temperatures. The single human activity of nitrogen fertilizer production provides more than half of all anthropogenic fixed nitrogen. Fertilizer is the fossil fuel of food. Fig. 1A displays 35 years of global nitrogen fertilizer use (1961–1995), disaggregated into 10 geographical regions (International Fertilizer Industry Association, http://www.fertilizer.org .). The rate of global nitrogen fertilizer use crossed 20 Mt(N) in 1965, 40 Mt(N) in 1973, and 60 Mt(N) in 1979. It remained within a band from 75 Mt(N) to 85 Mt(N) from 1986 to 1995, the consequence of continuous growth of consumption in Asia and a precipitous fall in consumption in the former Soviet Union and Eastern Europe. The plausibility of both saturation effects and upward pressures complicates attempts to predict future consumption of nitrogen fertilizer (10). The saturation in nitrogen fertilizer use in North America and Western Europe seen in Fig. 1A reflects fundamental physiological limits to yields and diminishing returns to single-factor inputs. A falling ratio of nitrogen fertilizer use to gross domestic product should be anticipated, inasmuch as nitrogen fertilizer contributes only to the production of a commodity and not to the downstream processing and services that account for an increasing fraction of wealth as incomes rise. By contrast, energy is a needed input at every stage in a complex economy, and hence has fewer built-in features leading to saturation. Saturation in fertilizer use will be reinforced as fertilizer subsidies are removed and external environmental costs are internalized in the fertilizer price. Other pressures act to counter saturation. Upward pressure on nitrogen fertilizer use will be felt, as latent demand in many developing countries is expressed. Fig. 1A shows that the growth in fertilizer use across the developing world has been very uneven, and comparisons of fertilizer use on the same crop across countries confirms that fertilizer use and yield are correlated (ref. 11 ; http://www.fertilizer.org/CROPS/ CROPS/harris.htm .). Upward pressure also will be felt if agricultural biotechnology continues to raise ceilings on yield potential with new crop variants dependent on nitrogen. Still other pressure may come from an expansion of fertilizer use on commercial forests and nonfood crops. As an alternative to fossil fuel, fast-growing energy crops may be established on dedicated, fertilized plantations. Nitrogen’s share, by weight, of total fertilizer (nitrogen plus phosphorus plus potassium) has climbed steadily; today, nitrogen’s share is about 60%, in sharp contrast to 1960, when roughly equal amounts of nitrogen, phosphorus, and potassium were applied. This phenomenon reflects a comparative advantage of nitrogen fertilizer resulting from both plant physiology and economics. It also reflects the unavailability of phosphorus or potassium in some parts of the world, leading to inappropriate ratios of application (ref. 12 and http://www.fertilizer.org/ PUBLISH/PUBENV .). It is interesting to compare the history of the use of nitrogen fertilizer and fossil fuels. Fig. 1B mimics Fig. 1A : the carbon content of fossil fuel use is shown for the same 10 geographical subregions and the same time period (ref. 50 ; Carbon Dioxide Information and Analysis Center, http://cdiac.esd.ornl.gov/ndps/ndp030.html ). Total global fossil-carbon use grew more slowly than total fertilizer use, crossing 3,000 million metric

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tons of carbon [Mt(C)] in 1965 and 4,000 Mt(C) in 1971, then remaining within a band between 4,800 and 5,100 Mt(C) from 1977 to 1984 and within a second band between 5,800 and 6,000 Mt(C) between 1988 and 1994. Growth of fossil-carbon use was slowed substantially by investments in energy efficiency.

FIG. 1. Comparable global data on release of nitrogen in fertilizer and release of carbon in fossil fuel, 1961–1995, with site of release disaggregated into 10 world regions. (A) Nitrogen in fertilizer; data from http://www.fertilizer.org . (B) Carbon in fossil fuel; data from http://cdiac.esd.ornl.gov/ndps/ndp030.html . Comparing Fig. 1 A and Fig. 1 B reveals that developing-country Asia gained global share more rapidly for nitrogen fertilizer than for fossil carbon. From 1961 to 1995, its nitrogen share climbed from 14% to 50% whereas its carbon share climbed only from 9% to 26%. In 1995, the nitrogen shares for North America and Western Europe were 15% and 12%, respectively, whereas the corresponding carbon shares were larger, 25% and 14%. In the former Soviet Union and in Eastern Europe nitrogen fertilizer fell far more than fossil-carbon use during the last years shown: In the former Soviet Union the 1995 level of nitrogen fertilizer use was 19% of the 1987 level, and in Eastern Europe it was 47% of the 1987 level, whereas the 1995 levels of fossil-carbon use were 70% and 63% of 1987 levels, respectively. Careful study of the fall in fertilizer use in the former Soviet Union and in Eastern Europe seems warranted. Land use. Land devoted to legumes, such as soybean and alfalfa, is the site of anthropogenic fixed-nitrogen production. Legumes are extraordinary, relative to other crops, in hosting nitrogen-fixing microorganisms in their roots; legumes are botanical fertilizers. At harvest, there is far more nitrogen in legumes than in other crops: soybeans are about 5% nitrogen (dry mass), wheat is 2%, rice is 1%. Land devoted to wet rice cultivation promotes asymbiotic nitrogen fixation, and thus is another site of anthropogenic fixed-nitrogen production. Schlesinger (5), citing Burns and Hardy (13) and including only legumes, estimates total anthropogenic land-use-related nitrogen fixation to be 40 Mt(N). Galloway (8), including both legumes and rice, makes the same estimate. Successive improvements in such estimates can be imagined, which compare preindustrial and contemporary nitrogen fixation rates for more and more kinds of land-use change. Included, for example, would be land converted from forests to fields. Land use also affects denitrification. Agricultural practices that reduce anaerobic environments, such as plowing (which aerates the soil) and draining wetlands, decrease denitrification, whereas irrigation increases denitrification. Denitrification also generally increases where fertilizer is applied, where legumes are planted, and where crops accelerate the mineralization of recalcitrant nitrogen in the soil. Greater burning of biological material also increases denitrification, because some of the nitrogen in biological material (wood, for example) recombines into N2 in flames, a process known as pyrodenitrification (2). The management of nitrogen, like the management of carbon, is likely to evolve from a focus only on sources to a balanced focus on sources and sinks. A strategy of engineered denitrification to reduce fixed-nitrogen build-up might ensue, based on manipulating land use to enhance natural denitrification processes. Presuming the simultaneous goal of managing the global greenhouse, such a strategy would entail only options with favorable ratios of wanted N2 to unwanted N2O. Combustion. Where the temperature of combustion exceeds about 1,500°C, there is enough concentrated energy to break apart atmospheric N2 and to form nitrogen oxides (14). Nitrogen oxide production also results as the “fuel nitrogen” in fossil fuels is burned. Estimating the rate of nitrogen fixation caused by anthropogenic combustion requires taking into account both the amount of combustion and the amount of pollution control. Control of nitrogen oxide emissions is increasingly widespread and increasingly strict.

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WHY THE INCREASE IN STOCKS OF FIXED NITROGEN IS TROUBLESOME Schematically, one can identify seven distinct adverse impacts of anthropogenic disruption of the nitrogen cycle, two expressed at the global scale and five at the regional scale. The two global impacts are caused by nitrous oxide in the atmosphere both contributing to the greenhouse effect and reducing the concentration of stratospheric ozone. Two of the five regional effects have direct impacts on public health: air pollution and unhealthy nitrate concentrations in drinking water. The other three regional effects are mediated by ecological processes: acid deposition, eutrophication of bays and estuaries, and ecosystem disruption resulting from uneven responses to nitrogen fertilization across species. These nitrogen effects can “cascade” (8). A nitrogen atom leaking away from an agricultural area can contribute to an air pollution problem over a city, then to a nitrate concentration problem in a municipal water supply, then to an acidification problem in a lake, then to a eutrophication problem in an estuary, and then to the destruction of ozone in the stratosphere. Such sequences, of course, can be interspersed with second passes through the agriculture and food system: through a cycle of fodder, cow, and manure, for example. I review each of the seven impacts briefly below. Note that in six of the seven instances (all except ecosystem disruption) a regulatory regime either is already in place or is being designed. Nitrous Oxide (N2O) Is a Greenhouse Gas. Because N2O has a long (120-year) residence time in the atmosphere and absorbs IR radiation, it is the one nitrogen gas emitted into the atmosphere that contributes significantly to the greenhouse effect: It is the fourth largest contributor to the natural greenhouse effect, after water vapor, carbon dioxide, and methane. The increase in N2O concentration since preindustrial times contributes about one-fifteenth as much to the greenhouse effect as the increase in CO2 concentration in the same period; about one N2O molecule has been added for every 3,000 CO2 molecules, but each is about 200 times as effective. Nitrous oxide is included explicitly in international climate agreements. Nitrous Oxide Depletes Stratospheric Ozone. The long atmospheric residence time of nitrous oxide is a consequence of its lack of reactivity in the troposphere and its very low solubility in water. Nitrous oxide is destroyed only in the stratosphere, where energetic UV light breaks it apart. One product of its decomposition is nitric oxide (NO), which acts catalytically to lower the concentration of stratospheric ozone (15). The engines of subsonic and supersonic aircraft traveling at high altitudes also emit nitric oxide in regions affecting stratospheric ozone. Current international assessments of the impact of aircraft nitric-oxide emissions on stratospheric ozone are expected to influence the near-term future of supersonic aircraft, as well as the regulatory regime for engine emissions of subsonic aircraft. Thus, because agriculture and aviation share common stratospheric chemistry, agriculture is enmeshed for the indefinite future in a high-stakes aerospace debate. Nitrogen Gases Generate Air Pollution. Because of their high reactivity in the atmosphere, nitric oxide (NO) and nitrogen dioxide (NO2), collectively called NOx, control the production of tropospheric ozone. Nitrogen gases (both ammonia and nitrogen oxides) are also precursors of very small particulates that travel long distances in the atmosphere and that find their way deep into the lung when inhaled (51). The regulation of NOx and tropospheric ozone is at the core of air pollution control in the United States. Emerging attention to very small particulates may lead to further regulations on nitrogen emissions. The Concentration of Nitrate Ions in Drinking Water Can Be a Threat to Infant Health. Nitrite ions (NO2−) in blood can inactivate hemoglobin, with dangerous consequences. The inactivation occurs because nitrite ions change hemoglobin, whose iron is doubly charged (Fe+ +) and can carry oxygen, into methemoglobin, whose iron is triply charged (Fe+++) and cannot carry oxygen. Infants younger than about 3 months are particularly at risk, for reasons that are not fully understood. The American Academy of Pediatrics speculates that fetal hemoglobin (which remains in the infant for the first few months of life) “may be more susceptible to oxidation to methemoglobin by nitrite” (ref. 16 ; see http://www.aap.org/policy/356.html ). Because the nitrite ions are formed in the gastrointestinal tract by the chemical reduction of nitrate ions (NO3−), the target of regulation is nitrate intake (17). The U.S. Environmental Protection Agency estimated in 1992 that 66,000 at-risk infants were drinking water whose nitrate concentration exceeded the U.S. health standard, 10 mg of nitrogen as nitrate (NO3−-N) per liter of water (18). Several water treatment options are available, all quite costly (18). Nitrogen Oxides Emitted into the Atmosphere Contribute to Acid Deposition. Acid deposition encompasses two related phenomena by which acidity is transferred from the atmosphere to the Earth’s surface: acid precipitation (including fog, rain, and snow) and dry deposition. The two principal contributors to acid deposition are nitrate and sulfate ions. Because precipitation is acidic even in the absence of air pollution (as a result of the effects of carbon dioxide and other gases on moisture in the atmosphere), acid precipitation is a term reserved for precipitation that is made still more acidic by pollution. Damage from acid deposition has been widely explored, and adverse consequences for lakes, forests, and buildings have been documented. To date, regulatory intervention to reduce acid deposition has focused far more on sulfate than nitrate, largely because a greater fraction of atmospheric sulfate arises from large emitters. High Nitrate Concentrations in Aquatic Ecosystems Can Lead to Eutrophication. Nitrogen is the limiting nutrient in many aquatic ecosystems, especially estuaries and bays, and thus the addition of nitrogen can lead to eutrophication, or excessive plant growth, followed by the depletion of dissolved oxygen and the development of aquatic “dead zones” where these plants decay (19). Because phosphorus, rather than nitrogen, is usually the limiting nutrient in fresh-water ecosystems, nitrate added to watersheds in their headwaters can be carried almost all the way to the sea before causing its first visible damage, thereby separating cause and effect both in space and time. An example is the hypoxic zone in the Gulf of Mexico off Louisiana, presumed to be brought about by agriculture in the Mississippi River watershed. A region defined by a dissolved oxygen concentration of less than 2 mg/liter, unable to sustain most forms of life, this hypoxic zone grows along the bottom of the gulf each summer as the gulf stratifies, plankton in abundance die and sink, and the dissolved oxygen at lower depths is consumed. The area of the hypoxic zone has been approximately 13,000 square km in recent years. In drought years the area is smaller and in flood years the area is larger, compelling evidence that something is carried into the gulf that promotes the growth and subsequent decay of plankton. Excess nitrogen from fertilized fields and livestock in the Great Plains is implicated. An interagency Mississippi River/Gulf of Mexico Watershed Nutrient Task Force has been established to assist policy-making (ref. 20 ; see also the Gulf of Mexico

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Hypoxia Assessment Plan at http://www.cop.noaa.gov/HypoxiaPlan.html ; † ). Nitrogen Addition to Ecosystems Reduces Biodiversity and Thereby Leads to Loss of Ecosystem Function. Both by air and water routes, fixed nitrogen deliberately applied to crops finds its way to unmanaged ecosystems, leading to their inadvertent fertilization. Schlesinger (21) writes: “Vegetation on much of the Earth’s land surface exists in a state of nitrogen deficiency, due in part to the low natural rate of nitrogen fixation and persistent losses of available nitrogen to denitrification and nitrate leaching. . . We know from a large ecological literature that the fertilization of natural ecosystems, perhaps first noted in the eutrophication of lakes, is likely to result in a loss of species diversity. . . Any addition of a resource to [a natural community where that resource is scarce] will lead to the dominance of the species that can use that resource most efficiently.” Rather than having a net positive effect, inadvertent fertilization alters ecosystem composition and diminishes ecosystem function (22–25).

LESSONS FROM CARBON AND ENERGY FOR NITROGEN AND FOOD Efforts already underway to manage human impacts on the carbon cycle suggest five principles that could guide first steps to manage human impacts on the nitrogen cycle: (i) reach agreement on goals relevant to sustainability; (ii) improve efficiency of producers and consumers throughout the system; (iii) harness market forces; (iv) incorporate mechanisms to learn continuously from research; and (v) engage the consumer and the citizen. In a properly crafted management system, these five prescriptions can be mutually supportive. Reach Agreement on Goals Relevant to Sustainability. Management of human impact on the nitrogen cycle has not yet reached the stage where goals have been agreed on. The goal of carbon cycle management, however, has been widely endorsed: stabilization of the climate. In ratifying the United Nations Framework Convention on Climate Change, the nations of the world agreed to pursue, collectively, not a constant total emission of carbon dioxide into the atmosphere but a constant level of carbon dioxide in the atmosphere. Constant stocks, not constant flows, were judged to define sustainability. Reasoning by analogy, the goal of nitrogen management would be ecological stabilization, reached through the achievement of constant stocks of fixed nitrogen in identified ecosystems. The stock in particular watersheds might be stabilized, as well as, perhaps, the total terrestrial stock. The goal of achieving a constant rate of production of fixed nitrogen would be rejected as inadequate. The implications of a goal of constant stocks are formidable. The goal of achieving a constant carbon dioxide concentration in the atmosphere makes future use of fossil fuels hostage to the combined power of natural and engineered carbon sequestration (26–29). Similarly, the goal of achieving constant stocks of fixed nitrogen makes future use of nitrogen fertilizer hostage to the strength of natural plus engineered denitrification in the corresponding ecosystems. Globally, until nitrogen fixation is balanced by denitrification, the amount of excess fixed nitrogen in the world will grow relentlessly, with increasing consequences for ecosystems and public health. In international negotiations, the choice of a specific target for the carbon dioxide concentration of the future atmosphere has been treated as separable from the decision that there should be such a target. The choice of a specific target is expected to require a depth of understanding of costs and benefits that may not be available for several decades. Meanwhile, there is broad-based participation in “what if” discussion of specific targets for the atmospheric carbon dioxide concentration. Similarly, choosing the specific ecosystems whose total fixed nitrogen is targeted, and the targets themselves, is premature, but “what if” discussion is already timely. Improve Efficiency of Producers and Consumers Throughout the System. The flow of nitrogen through the food system can be measured in various ways. By one measure, already discussed, the food system elicits an incremental fixation of 120 Mt(N)/yr in the form of chemical fertilizer and legumes. By another measure, 50 Mt(N)/yr is the flow of nitrogen that rides along with the annual global harvest of 2,600 Mt (dry weight) of crops (mid-1990s estimates); not included is the nitrogen in forage consumed by grazing animals (7). By a third measure, the nitrogen flow in the daily intake of food is about 23 Mt(N)/yr, the sum of 17 Mt(N) in plant food and 6 Mt(N)/yr in animal food (7); assuming that protein is 16% nitrogen and that there are 6 billion people, this works out, plausibly, to an average of 66 g of protein per person per day. Thus, less than half of the fixed nitrogen added by agriculture ends up in our harvested crops, and less than half of the fixed nitrogen in our harvested crops ends up in what we eat. Tracking material flows through a system containing both producers and consumers, documenting leakage at each stage, is an application of industrial ecology (30, 31). To categorize ways of reducing nitrogen leakage, Galloway (32) suggests that all leakage be assigned to either crops, animals, or people. An ideal system would return all crop wastes, manure, and food wastes to the field, and no nitrogen would be lost through volatilization, runoff, or denitrification. As a result, maintaining constant food production would require no external inputs of nitrogen. Cohen (33) sets forth a similar utopia: “Required agricultural inputs of nutrients and energy [within half a century] will be derived from human, animal, and industrial wastes rather than from today’s fertilizers and fossil fuels. Unwanted effluents like eroded soil or agricultural runoff with pesticides and fertilizers will be eliminated or converted to productive inputs for industrial and urban use.” Galloway’s or Cohen’s ideal system could have low throughput, in which case it would somewhat resemble preindustrial agriculture. But what is desired is high throughput, and no such system has ever been attempted. Any close approach to a high-throughput, zero-loss system would incur unacceptable costs for transporting wastes back to the field and probably would stress soil unacceptably. Nonetheless, the zero-loss system provides a useful point of reference from which to explore improved nitrogen-use efficiency in the crop system, the animal system, and the food consumption system. Crops. Of the many losses of fixed nitrogen in the crop system, probably the most important are the losses associated with suboptimal application of fertilizer. A report of the National Research Council (34), in the interest of pedagogy, set forth a representative relationship between fertilizer application rate and yield for a corn field. The yield is 4 metric tons per hectare (t/ha) in the absence of fertilizer, 7 t/ha when fertilizer is applied at 100 kg(N)/ha, and 8 t/ha when fertilizer is applied at 200 kg(N)/ha. “Thus, the first hundred kg of nitrogen per ha is three times as effective as the second hundred in adding to yield. . . The model can be taken further. Corn contains about 1.3% nitrogen. Thus the harvested grain retains 39 of the first 100 kg of nitrogen added as fertilizer, but only 13 of the second 100” (2). Efficiencies of 13% suggest a large potential for improvement through social and technical innovation. Diminishing returns to scale for a single factor of production suggest a sensitivity to price-related policy. The opportunity for knowledge to substitute for nitrogen at the field is abundant. In precision agriculture, timing, quantity, and chemical form are controlled at the subfield level. Even within the constraints of traditional farming, there are measurable benefits from revising the timing of delivery (35) and

†Scavia,

D., Workshop on Materials and Energy Flows, United States Geological Survey, November 3, 1998, Reston, VA.

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fine-tuning the quantity applied to reflect soil variability (36). Smil (7) estimates that the “cumulative effect of adopting well-proven and lowcost measures aimed at increasing efficiency of nutrient uptake” would expand the effective global supply of nitrogen fertilizer by about 20 Mt (N)/yr. About half of the increment would come from improved fertilizer management and about half from reducing erosion, expanding the use of nitrogen-fixing crops, and increasing the recycling of organic wastes. Animals. Of the many losses of fixed nitrogen in the animal system, probably the most important are the losses associated with the nitrogen in manure. Geographic separation of feed-lots and dairies from sites of crop production, a relatively recent phenomenon, has greatly raised the cost of recycling animal wastes. Even though consolidation of livestock management into large commercial units reduces collection costs, transportation costs make loop-closing uneconomic. With the Netherlands in the lead, public policy is forcing new management strategies for manure that are more responsive to environment and public health. As per-capita income rises in most countries, this inefficiency grows in importance, because an increasing fraction of the flows of nitrogen from plants to people involves animals as intermediaries. In recent years, 40% of global grain production has gone to animal feed, but in the United States this fraction is 70%, and in Asia it has climbed in the last decade (1985–1987 versus 1995–1997) from 15% to 24% (37). There is a parallel in the energy system: as income rises, an increasing fraction of fossil fuel energy reaches the consumer through the intermediary of electricity. Meat is the electricity of food. Food consumption. There are losses of fixed nitrogen throughout the food system: in the ships and trucks transporting food, in the markets where it is sold, and in the kitchens and restaurants where it is prepared. Neither the most important losses nor the losses most easily reduced are easily identified. Any analysis of nitrogen flows through the food system must take cultural factors into account. “Culture . . . defines which biological raw materials are seen as food and which are not” (33). For most of the world’s people, eating is a form of pleasure, enhanced by variety and free choice. In response, agriculture becomes more varied and more international. Overeating looms large. How much nitrogen is required in food? The nutritionists’ recommended protein requirements (effectively, nitrogen requirements) have dropped over time, as knowledge has improved and as the ideal of a child growing as big as possible has been recognized to be a cultural construct. Sasson (38) writes: “It is not necessary to enjoy good health to have a diet where proteins represents 15% or more of the total caloric intake. A much lower proportion (5% in the case of good quality proteins such as those in eggs or milk, or 8% in the case of other types of proteins) is sufficient to cover the needs of an individual, child or adult, as long as he has an adequate calorie intake as well. Human milk contains only 5–6% of its energy in the form of proteins and yet it is an ideal food for the newborn child.” The global grain yield (60% of all food production) has had almost the same nitrogen intensity (nitrogen percent by weight) over the past three decades, because the rates of growth of production of wheat, rice, and corn, each with its distinct nitrogen intensity, have been almost identical, about 2.5% per year (39). There appears to be no trend analogous to the “decarbonization” of the energy economy, the continuous decrease in the average carbon content of fuel throughout the 20th century that resulted from coal losing market share to petroleum and then petroleum losing market share to natural gas. Harness Market Forces. A general message from theory and experience is that market mechanisms are efficient. They stimulate the collective imagination, which is inevitably more powerful than the imagination of any small set of people who try to discern constructive behaviors on their own. Market mechanisms affect both producers and consumers. Market mechanisms reward those who do more than they need to do, relative to some yes-no measure of compliance. The “fertilizer sector” has not heeded this message. Instead, it “has been characterized by protection, subsidies, and price controls” (40). Among the market mechanisms available for nitrogen management are cap-and-trade regimes, where a specified number of permits to fix nitrogen are issued and traded (41). Arguments in favor of setting caps on fixed-nitrogen inputs to a given region are beginning to be marshaled (42). The permit system could be organized at the watershed level, the national level, or the international level. A cap-and-trade precedent at the national level is the tradable permit system for atmospheric sulfur dioxide emissions from U.S. coal-fired power plants. The regime’s first years have been unexpectedly successful (43). This particular trading system had features that enabled it to survive a politically charged design process: it involved only a small number of traders (on the order of 100), the measurement of emissions was relatively straightforward, and the political consensus that made enforcement credible was in place. The U.S. has no cap-and-trade system for NOx emissions, even though the principal motivation (reducing acid precipitation) is the same. Beginning with trading in NOx emissions is a sensible way to gain the experience necessary to implement full-scale trading in fixed nitrogen. Isn’t more expensive food the inevitable consequence of policy interventions to address previously ignored environmental impacts of agriculture? And isn’t more expensive food a scourge on the poor? Experience in the energy sector suggests two ways out of this trap. First, when priority is given to new problems, new ideas emerge; tradeoffs turn into joint gains. One learns to produce food more cheaply and with reduced environmental consequences. Second, general subsidies can be replaced by targeted subsidies for the poor. In the regulated rate schedules for electricity, the first few units of consumption (the first 100 kilowatt hours per month, for example) often are subsidized. Such “lifeline rates,” in both industrialized and developing countries, are a clever mediator between efficiency and equity, because the limited fraction of total use by poor families makes the impact of lifeline rates minimal (44). Incorporate Mechanisms to Learn Continuously from Research. Crop physiology and ecophysiology have been identified as areas of agricultural science that hold the key to substantial expansion of global food supply. Basic understanding of the soil-crop interactions that govern yield in today’s most productive regions should permit greater “ecological intensification,” higher “input end-use efficiency” and better protected “natural resource quality” (36). Basic understanding of soil-crop interactions also should permit crops to be grown safely for the twin objectives of food (or feed) and energy, a strategy of interest in both industrialized and developing countries. The food component of a plant and the residue would be managed jointly, informed by a detailed understanding of how much residue should be returned to the land. Wherever, in high-yield agriculture, the soil’s need for carbon could be satisfied by a fraction of the total carbon in residues, the rest of the carbon in residues would be freed for commercial use. Today’s practice of burning residues on the field could be replaced by high-technology processing of residues for electricity and fuels (45). And if more of the nitrogen must be returned to the soil than would come along with the residues recycled for carbon, then the nitrogen and the carbon in the unrecycled residues might be unbundled and managed separately, the nitrogen meeting the needs at the field of origin, and, if some is left, serving as fixed-nitrogen input elsewhere. The requirements of the soil

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for other nutrients and micronutrients also would have to be met. At the intersection of agricultural and environmental science, the priority is to understand the transport and fate of nitrogen nutrient, as well as the ecological consequences of increased nitrogen input (24). In nitrogen-cycle research there is a “missing fixed-nitrogen problem” analogous to the “missing carbon” problem in global climate research: little is known about the rate at which anthropogenic fixed nitrogen is denitrified in terrestrial and aquatic ecosystems (8). The recent result that terrestrial sinks for atmospheric carbon dioxide, per unit area at the continent level, are larger than ecologists expected (46) provides further reason to understand how nutrient-enriched ecosystems evolve over time. If, for example, 50 Mt(N)/yr of today’s anthropogenically fixed nitrogen (about one-third of the total) were forming recalcitrant organic compounds at a C/N mass ratio of 20:1 (a molar ratio of 23:1), carbon would be sequestered in organic matter at a rate of 1,000 Mt(C)/yr, onesixth of the current rate of carbon emissions from fossil fuels. Economists and agronomists are locked in debate about likely future yields. In the energy world, economists and geologists are locked in virtually the same debate, this time about likely additions to reserves of fossil fuels. The reason for lack of resolution is the same. The historical record shows a run of successes (higher yields, new reserves) for many decades. Because the method of the economists is to predict future outcomes from past performance, economists expect success to continue. And because for the scientists future success depends on discoveries they will have to make and do not now know how to make, the scientists are doubtful. At its core, this disagreement is about the pace of technical change. Agronomists are the geologists of food. Engage the Consumer and the Citizen. In the early 1970s the previously separate concerns for energy production and energy use merged into a single inquiry. The oil field, the gasoline station, the car engine, and alternatives to commuting to work now were linked. The system was further enlarged by thinking of the consumer not as someone who devours a certain amount of energy but as someone who has to be provided a service or amenity, such as transportation or lighting or a warm space. In the case of the agriculture and food system such a merger would integrate the perspectives of the agronomist and the nutritionist, the farmer and the eater. The protein consumption of large numbers of ever better fed people dominates the impacts of food consumption on the nitrogen cycle. Consider what the Food and Agriculture Organization reports about the 110-g daily protein consumption of the average American. Of the 40 g of vegetable protein, 25 are from grains, and 15 are from other sources. Of the 70 g of animal protein, 40 are from meat, 20 from milk, five from eggs, and five from fish and seafood (Food and Agriculture Organization of the United Nations, http://apps.fao.org/lim500/nph-wrap.pl? FoodBalanceSheet&Domain=FoodBalanceSheet ). This diet is beckoning the rest of the world (47). Food preferences, beliefs about healthy eating, social norms, ethical constraints such as a concern for animal welfare: these are among the factors that determine how our eating disrupts the nitrogen cycle. The individual is not only an eater but a citizen. Here energy again is a guide, this time to political discourse. Desire for autonomy drives interest in solar energy. Mistrust of expertise fuels arguments against nuclear power. Organic farming is the solar energy of food. Agricultural biotechnology is the nuclear power of food. Agricultural biotechnology is at risk of repeating the course followed by nuclear power. Those in charge believe the way to deal with the public’s qualms is “to educate,” but listening would be more productive. The stakes are high. The development of nitrogen-fixing corn and wheat, for example, could transform nitrogen management, but with what other consequences? Questions burgeon: How well understood is the underlying science, and how quickly is the science becoming better known? Where are the irreversibilities? If scientists are the guardians, who guards the guardians? And who protects all of us from guardians of the guardians who see their task as avoiding every potentially slippery slope, thereby annulling the spirit of experimentation so critical to our future?

CONCLUSIONS Through numerous feedback loops the impacts of agriculture on the environment become impacts of agriculture on agriculture. Impacts on both the nitrogen and the carbon cycle result in changes in climate, changes in soil characteristics, changes in species mix, changes in pest populations, some of which will benefit agriculture, but many of which will not. Indeed, the existence of these closed loops is one of the principal reasons why impacts of agriculture on the environment merit the attention of the agriculture community. The finding that the nitrogen cycle at several spatial scales is strongly impacted by food production should not surprise us. Consistently, when one investigates the effects of aggregate human activity on the natural world, one finds ecological systems that are stressed by this activity. Consistently, one finds that these stresses are only partially understood, that built-in self-correcting mechanisms to keep these stresses from becoming dangerous are largely absent; that deliberate mitigating actions are not hard to find once the problem receives sustained attention; and that at least some of the mitigating actions that emerge from such an exercise are ethically complex. The societal response to the new knowledge that abundant fixed nitrogen produces negative environmental effects has been appropriately cautious. Nitrogen fertilizer, along with improved seed and irrigation, are the “technological trinity” responsible for the high-yield agriculture of the Green Revolution (40). High-yield agriculture, in turn, has been key to avoiding mass starvation in much of the world. Poorly devised strategies to reduce the use of fertilizer could lead, in the short term, not only to human distress but also to environmental adversity, were such efforts to result in production, on the margin, from lands relatively vulnerable to environmental damage (land on steep slopes, wetlands). Nonetheless, it is inevitable that the agriculture and food system will evolve to contain its impacts on biogeochemical cycles. As rational policy regimes replace more opportunistic ones, the agriculture and food system will be subject to the same governance as other industrial systems (48, 49). At the level of the field, greater inputs of information and fewer inputs of chemicals (including nitrogen fertilizer) are a likely outcome. Management of the nitrogen cycle can be informed by the greater experience to date in managing the carbon cycle. There are familiar objectives, uncertainties, environmental risks, and collisions of values. Among the promising approaches are: (i) setting a goal of ecosystem stabilization; (ii) searching the entire production and consumption system for opportunities to improve efficiency; (iii) implementing cap-andtrade systems for fixed-nitrogen; (iv) expanding research at the intersection of agriculture and ecology, and (v) focusing on the food choices of the prosperous. Coordinated management of the nitrogen and carbon cycles is required to address key environmental issues. The global increase in fixed nitrogen may be fertilizing the Earth, transferring significant amounts of carbon from the atmosphere to the biosphere, and mitigating global warming. A modern biofuels industry someday may produce biofuels from crop residues or dedicated energy crops, reducing the rate of fossil

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fuel use, while losses of nitrogen and other nutrients are minimized. A basic research program that addresses the critical scientific questions today limiting agricultural productivity is likely to address nitrogen fertilization and biomass energy as well. The agriculture and food community can be expected to resist external pressure. However, the long-run consequence of this pressure is likely to be beneficial. A new challenge stimulates fresh approaches that result in greater efficiency, here, in particular, in managing fixed nitrogen. Greater efficiency will reduce both the external intrusion and the impact on costs. 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