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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Table of Contents

Climate change and carbon dioxide: An introduction Charles D. Keeling

8273–8274

Tribute to Roger Revelle and his contribution to studies of carbon dioxide and climate change Walter H. Munk

8275–8279

Equilibration of the terrestrial water, nitrogen, and carbon cycles David S. Schimel, B. H. Braswell, and W. J. Parton

8280–8283

Potential responses of soil organic carbon to global environmental change Susan E. Trumbore

8284–8291

Global air-sea flux of CO2: An estimate based on measurements of sea–air pCO2 difference Taro Takahashi, Richard A. Feely, Ray F. Weiss, Rik H. Wanninkhof, David W. Chipman, Stewart C. Sutherland, and Timothy T. Takahashi

8292–8299

Characteristics of the deep ocean carbon system during the past 150,000 years: ΣCO2 distributions, deep water flow patterns, and abrupt climate change Edward A. Boyle

8300–8307

Direct observation of the oceanic CO2 increase revisited Peter G. Brewer, Catherine Goyet, and Gernot Friederich

8308–8313

The observed global warming record: What does it tell us? T. M. L. Wigley, P. D. Jones, and S. C. B. Raper

8314–8320

Possible forcing of global temperature by the oceanic tides Charles D. Keeling and Timothy P. Whorf

8321–8328

Spectrum of 100-kyr glacial cycle: Orbital inclination, not eccentricity Richard A. Muller and Gordon J. MacDonald

8329–8334

Can increasing carbon dioxide cause climate change? Richard S. Lindzen

8335–8342

Gases in ice cores Michael Bender, Todd Sowers, and Edward Brook

8343–8349

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Tree rings, carbon dioxide, and climatic change Gordon C. Jacoby and Rosanne D. D'Arrigo

8350–8353

Geochemistry of corals: Proxies of past ocean chemistry, ocean circulation, and climate Ellen R. M. Druffel

8354–8361

A long marine history of carbon cycle modulation by orbital-climatic changes Timothy D. Herbert

8362–8369

Dependence of global temperatures on atmospheric CO2 and solar irradiance David J. Thomson

8370–8377

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CLIMATE CHANGE AND CARBON DIOXIDE: AN INTRODUCTION

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Proc. Natl. Acad. Sci. USA Vol. 94, pp. 8273–8274, August 1997 Colloquium Paper This paper serves as an introduction to the following papers, which were presented at a colloquium entitled “Carbon Dioxide and Climate Change,” organized by Charles D. Keeling, held November 13–15, 1995, at the National Academy of Sciences, Irvine, CA.

Climate change and carbon dioxide: An introduction

CHARLES D. KEELING Scripps Institution of Oceanography, 10666 North Torrey Pines Road, La Jolla, CA 92037

© 1997 by The National Academy of Sciences 0027-8424/97/948273-2$2.00/0 PNAS is available online at http://www.pnas.org. Since the dawn of history, human beings have had the ability, superior to all other living beings, to exploit the Earth's environment to their own immediate advantage. For most of human history the consequences were only of local or regional significance. Over the past century, however, the rapid rise in population and the increasing intensity and scale of human enterprises have made it possible for humans to alter the Earth on a global scale. One important measure of human activity is the rate of utilization of energy. This rate has accelerated strikingly in the past hundred years because of rapidly increasing human population coupled with increasing per capita energy consumption. Is it possible that accelerating human activity has already caused globally significant environmental change, or is about to do so? One aspect of this question relates to possible human alteration of the Earth's climate, which is essentially the summation of weather and its variability. Although climate clearly varies with latitude and elevation and with physical and ecological features, such as deserts and forests, it once was considered to be constant over time. We now know, however, that weather does vary on long time scales and, therefore, that climate is variable. Climate has indeed varied profoundly, as evidenced by proxy records indicating a succession of ice ages and warm “interglacial” eras over the past million years. Proxy records also reveal climatic variability on time scales of hundreds to thousands of years. Long-term weather records even show evidence of significant variability over decades, which may be associated with climatic change. This short-term variability makes it difficult to separate out subtle climate changes that might be caused by accelerating human activities. Short-term climatic change was discussed recently in a National Research Council (NRC) workshop: Natural Climate Variability on Decade-toCentury Time Scales (1). By comparing past climatic conditions with recent ones, it was not clear whether human activities have altered climate or not. Better data and a better understanding of the causes of climatic variability are needed to decide this. Broadly speaking, climatic change is caused by exchanges of energy, momentum, and chemicals between the atmosphere, the oceans, and land surfaces. Oceanic and atmospheric circulation, turbulent mixing, photochemistry, and radiative transfer are all involved. These processes are mainly natural, but some, at least, are susceptible to human influence. Processes that involve the so-called greenhouse gases are probably the most critical candidates. These greenhouse gases, mainly carbon dioxide but including others such as methane, nitrous oxide, and halocarbons, enter the air mainly as byproducts of the combustion of coal, natural gas, and petroleum, and to a lesser degree through other industrial and agricultural activities. Their rates of emission into the air are roughly proportional to the global rate of energy consumption arising from human activity. Thus, as human population and per capita energy consumption have increased, concentrations of these gases have risen in nearly direct proportions to the product of both increases. As they build up, these gases trap radiation upwelling from the Earth's surface. The expected consequence is rising temperature at the Earth's surface unless some compensating process cancels out this tendency. Whether such compensation is occurring is presently a matter of debate. Carbon dioxide deserves attention as a greenhouse gas because it is indisputably rising in concentration. To understand what controls its abundance in the atmosphere, and hence its influence on the greenhouse effect, we must address all the processes that affect, and are affected by, its concentration in the atmosphere. These processes include its interactions with the chemically buffered carbonate system in seawater and with vegetation because of its vital role in photosynthesis. The sum of all processes affecting carbon on the Earth, and hence controlling the concentration of atmospheric carbon dioxide, is called the “carbon cycle.” We need to understand how the carbon cycle functions in order to know how human activities may affect carbon dioxide. Although the pathways of carbon through the global carbon cycle are understood in general, knowledge of the actual rates of change of the fluxes between the atmosphere, land, and ocean is less advanced. The annual anthropogenic carbon input to the atmosphere between 1980 and 1989 has been estimated (2) to include 5.5 ± 0.5 GtC (thousand million metric tons of carbon) from fossil fuel combustion and 1.6 ± 0.6 GtC from land-use change, yielding a total of 7.1 ± 1.1 GtC. Of this annual input, 3.3 ± 0.2 GtC remained in the atmosphere, and 3.8 GtC were removed. Oceanic uptake, related to carbonate buffering, is thought to account annually for about half of the removal. Regrowth of northern hemisphere forests has been estimated to account for perhaps 0.5 ± 0.5 GtC. The removal mechanisms of the remaining carbon, 1.3 ± 1.5 GtC per year, are uncertain. This residual term is commonly referred to as the “missing carbon sink.” It must be located and the uncertainty in the other individual terms in the global carbon cycle must be reduced if the extent of human impact on the carbon cycle is to be assessed reliably. Furthermore, a feedback mechanism exists whereby climate change may itself alter the carbon cycle. For example, widespread warming from increasing greenhouse gases may change the rates of uptake of carbon dioxide by the oceans globally and may alter gas exchange with vegetation. Even less is known about such feedback mechanisms than is known about the missing carbon sinks. To review progress in our understanding of the carbon cycle and climate, the National Academy of Sciences (NAS) supported the colloquium summarized in this volume. In planning for it, special attention was given to highlighting a portion of

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the illustrious career of the late Roger Revelle, a long-time NAS member and contributor to many NRC activities. The paper by Walter Munk that follows presents a detailed description of Revelle's career. My contacts with Roger Revelle, although less intimate than Walter Munk's, spanned nearly four decades, and left on me an indelible impression of one of the great figures in post-World War II science. Roger believed that science should be not only useful, but also enjoyable; that scientists should be held in high regard and should be allowed to follow their own leads in the quest for scientific knowledge with as much freedom as possible. Roger began his career as a chemist studying carbon in the oceans. During the years that I knew him he maintained an interest in the global carbon cycle, while making highly significant contributions in several other fields. It has been a great pleasure for me to have taken part in this colloquium on a subject in which Roger took keen interest throughout his career. He would have enjoyed attending, and we would have benefited from his wisdom as many of us did during his lifetime. With only our memories of him we have nevertheless tried to live up to his standards by steadfastly addressing important topics in a manner both useful and enjoyable. Fifteen refereed articles are included in this volume. Some of these papers review previous studies, while others present new data and analyses. All address topics in which Roger was keenly interested: (i) the extent to which climate is changing owing to both natural causes and human activities, (ii) whether these changes, in part, are long-term manifestations of increasing carbon dioxide, and (iii) how the oceans, terrestrial plants and soils, and atmosphere function in general as a necessary foundation for exploring the first two topics. The spirit of this offering is to advance knowledge so that all people will have a rational basis for dealing with environmental problems, especially those that mankind may have created. This mission is consistent with Revelle's optimistic belief that the human race, given the opportunity through enlightenment, will naturally serve its own best interests, and that people able to contribute to this enlightenment will do so zealously and unselfishly, as Roger did. Special thanks are owed to the committee that assisted me in planning this colloquium and in handling the review process: Peter Brewer, Ellen Druffel, Edward Frieman, Robert Knox, Walter Munk, Taro Takahashi, and Karl Turekian. In addition to funding from the NAS, the colloquium was supported by five federal agencies: the National Science Foundation, the National Oceanic and Atmospheric Administration, the Office of Naval Research, the U.S. Department of Energy, and the National Aeronautics and Space Administration. The planning committee members are grateful for this support and to Neil Andersen, formerly of the National Science Foundation, who played a key coordinating role. We also thank the National Research Council's Ocean Studies Board (OSB) and its staff, who helped us to make this colloquium a success, especially Ed Urban of the NRC for assistance in very many aspects of the preparation for the meeting and this volume of papers. Roger Revelle's significant positive influence on the NRC and OSB over many years was demonstrated by the NRC staff's enthusiasm for and dedication to this enterprise. 1. National Research Council (1996) Natural Climate Variability on Decade-to-Century Time Scales (National Academy Press, Washington, DC). 2. Intergovernmental Panel on Climate Change (1996) in Climate Change 1995: The Science of Climate Change, eds. Houghton, J. T., Meira Filho, L. G., Callander, B. A., Harris, N., Kattenberg, A. & Maskell, K. (Cambridge Univ. Press, New York), p. 17.

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Proc. Natl. Acad. Sci. USA Vol. 94, pp. 8275–8279, August 1997 Colloquium Paper This paper was presented at a colloquium entitled “Carbon Dioxide and Climate Change,” organized by Charles D. Keeling, held November 13–15, 1995, at the National Academy of Sciences, Irvine, CA.

Tribute to Roger Revelle and his contribution to studies of carbon dioxide and climate change WALTER H. MUNK Institute of Geophysics and Planetary Physics, University of California at San Diego, La Jolla, CA 92093-0225

© 1997 by The National Academy of Sciences 0027-8424/97/948275-5$2.00/0 PNAS is available online at http://www.pnas.org. I first came to Scripps Institution of Oceanography (SIO) in the summer of 1939, after completing my junior year at the California Institute of Technology. Roger Revelle was 30 years old, with the rank of instructor (long since abolished by the University of California), and a lieutenant junior grade in the Naval Reserve. Roger invited me to come along on an experiment to measure currents in the waters over the California borderland. The standard tool was an Ekman Current Meter; for every 100 revolutions of a propeller, a 2-mm ball is dropped into a compass box with 36 compartments, each corresponding to a 10° segment in current direction. The trouble was that the balls would not fall into the compartments. Roger was up all night doggedly fussing with the current meter until, at breakfast time, the release was functioning. This is my earliest memory of Roger. Scripps and the War Years After taking up geology at Pomona College under the legendary teacher Alfred “Woody” Woodford, followed by a graduate year at University of California at Berkeley, Roger came to Scripps in 1931 to study deep-sea muds. By 1936 he had completed his thesis, “Marine Bottom Samples Collected in the Pacific Ocean by the Carnegie on Its Seventh Cruise,” and stayed on as an instructor (Fig. 1). During his year at Berkeley, Roger married Ellen Clark, a grandniece of E. W. Scripps and Ellen B. Scripps, after whom the Scripps Institution of Oceanography was named. After a year at the Geophysical Institute in Bergen, Norway, he returned to Scripps. Roger went on active naval duty 6 months before the bombing of Pearl Harbor and stayed in the Navy for 7 years. He was instrumental in organizing the Office of Naval Research. In 1946 he was officer in charge during Operation Crossroads of the geophysical measurements taken during the atomic bomb tests at Bikini Atoll. None of the participants will ever forget this experience. For many years, Roger contributed to the understanding of the environmental effects of radiation and to questions of disposal of atomic wastes at sea (1). [Revelle contributed to the report in ref. 1 as Chairman of the National Academy of Sciences Panel on Biological Effects of Atomic Radiation (BEAR).] I suspect that Roger's participation for so many years, from 1958 to 1981, in the Pugwash Disarmament Conferences can be traced to the Bikini bomb tests. The Scripps Directorship After more than 40 years as a local marine station, Scripps Institution had agreed to undertake a program to study the disappearance of sardines from California waters (Fig. 2). This involved the commissioning of two vessels. Scripps Director Harald Sverdrup was anxious for Roger to return to La Jolla to succeed him as director of Scripps. Sverdrup (2) wrote, “regardless of the capacity in which you return here, you are the logical man to take charge . . . of the work at sea.” And Roger (3) agreed: Sverdrup's support for me as successor is also based upon the fact that I am practically the only person available who has had extensive experience at sea, in particular in the organization and carrying out of expeditions. He feels that Scripps must be, at least in part, re-oriented toward work on the high seas rather than the inshore and laboratory type of research which is being largely done at present. Sverdrup's statement “regardless of the capacity in which you return” was a reference to a developing opposition to Roger as the next director. One Scripps professor complained that Roger was too untidy to be trusted with administration (3), noting that he “just let everything pile up on his desk” and “was to easily diverted.” Again Roger agreed (3), referring to his own “obvious and numerous weaknesses, such as a tendency to procrastinate, to take on too many obligations, not to delegate authority, to be high-handed.” The outcome was that Carl Eckart was appointed director of Scripps in 1948, and Roger was appointed associate director with the expectation to succeed Eckart in a few years. It wasn't that easy! A 1950 letter to University of California President Robert Sproul (4), signed by more than half the Scripps faculty, states: We understand that the impression has been gained in some quarters that opposition is vanishing at Scripps Institution to Dr. Revelle as a candidate for Director. We assure you that whereas we have a high regard and friendship for him, we feel as strongly as before that his appointment . . . would not be in the interest of the institution. His recent administrative actions confirmed our conviction. Roger was appointed director in 1950. It is a tribute to Roger's disdain for pettiness that some years later one of the writers referred to Roger's “brilliant Directorship” (13). The Heady Expedition Days The era opened in 1950 with the Mid-Pacific expedition into the equatorial waters of the central Pacific Ocean. This was followed in 1952–1953 by an extended voyage to the South Pacific, which was called Capricorn. Both expeditions were led personally by Roger. It was discovered that only a thin veneer of sediments overlies the solid rock, that the heat flow through the sea floor is about the same as that on land, and that the flat-topped seamounts at a depth of 2,000 m had been volcanic islands less than 100 million years ago. All of this spoke for great mobility of the “solid” Earth. When Roger and his

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colleagues tried to core and dredge the Tonga Trench, the instruments came up battered and bent, and empty. If there were any sediments, they were sparse and thin. The observations could best be explained if the rocky sea floor was disappearing into the Earth along the axis of the trench (this is now called subduction). On Capricorn, Ronald Mason towed a magnetometer behind the vessel and recorded a complicated set of wiggles that no one could understand. Later Mason produced a map of the magnetic field under the sea floor showing stripes of normal and reverse magnetization.

FIG. 1. Roger Revelle as an instructor at Scripps (circa 1936). Photo by Eugene LaFond. [Reproduced with the permission of the SIO Archives, UCSD.] With hindsight, the evidence was all there for proclaiming the doctrine of plate tectonics. And when, 10 years later, the puzzle was put together, Scripps unfortunately did not play a leading role. Still, I think of the 1950s as the great era of the Institution. When Roger left in 1961, Scripps had a Navy bigger than that of Costa Rica. Greenhouse Even as he led the exploration of the Pacific, Roger was active for several years in promoting the International Geophysical Year (IGY). In 1956 he became chairman of the IGY Panel on Oceanography. That same year, Charles David Keeling joined the Scripps Institution staff to head the IGY program on Atmospheric Carbon Dioxide and to start the measurements at Mauna Loa and Antarctica. And that is why we are here 40 years later. Keeling credits Harry Wexler and Roger Revelle for insisting on the continuity of the measurements; such time series are few and far between and worth their weight in gold. In 1957, Roger and Hans Suess demonstrated that carbon dioxide had increased in the air as a result of the consumption of fossil fuels, in a famous article published in Tellus (5). Roger's interest in CO2 was to engage his attention for the rest of his life. In 1965, the President's Science Advisory Committee Panel on Environmental Pollution under Roger's leadership published the first authoritative report that recognized CO2 from fossil fuels as a potential global problem (6). Public opinion was influenced through a widely read article in Scientific American (7). Roger participated in the exploration of the atmospheric greenhouse problem from the 1950s, when it was a cottage industry for a few academics, to the 1990s, when global climate change involved industry and government on an international scale. He once estimated that he had spent 20% of his time keeping current with the issues. THE MOHOLE PROJECT In 1957 Roger and I were among a group that called themselves the American Miscellaneous Society (AMSOC). AMSOC promoted an attempt to drill through the ocean floor into the Earth's mantle. A test off Guadalupe Island successfully drilled through 200 m of sediments into the basalt in water 4,000 m deep, demonstrating the feasibility of “dynamic positioning.” This MOHOLE project (Fig. 3) eventually failed because of poor Washington management but led some years later to the successful Ocean Drilling Program. Ocean Leadership The U.S. ocean program was then firmly in the hands of three men: Maurice Ewing, Columbus Iselin, and Roger Revelle. There has not been a comparable ocean leadership since those days.* While Revelle served as a founding member of the National Academy of Sciences Committee on Oceanography (NASCO), the funds budgeted nationally for oceanography rose from $12 million in 1957 to $97 million in 1960. Roger played a major role in organizing the IGY and in forming the Scientific Committee for Ocean Research (SCOR) and the International Oceanographic Commission (IOC), and then served as Chairman of a joint IOC/SCOR Committee on Climate Changes and the Ocean. These organizations continue to play an important role in international oceanography. Roger enjoyed an international reputation as oceanographer in the 1950s but became better known to the greater scientific community and to the public through his work for the National Academy of Sciences as a science spokesman with broad knowledge of the environment. He worked very hard behind the scenes to frame the important scientific questions and then to secure the resources to answer them. Policy makers looked to him for a reasonable assessment of which scientific problems should take priority. Scientists sought his advice and support to focus research and get it funded. Congressman Emilio Daddario (8) has remarked on Roger's “combined experience, intelligence and good judgment about issues.” Building the University of California at San Diego (UCSD), 1954–1961 In parallel with these developments came the beginnings of the UCSD. No oceanographic program, Roger said, could maintain intellectual excellence for more than a generation without an attachment to a great university. The obvious site was some 1,100 acres of largely undeveloped public land just to the north of the Scripps Institution of Oceanography. Fortuitously, Roger's initiative coincided with a new master plan for the

*This may have changed; in the last several years, Admiral (U.S. Navy, ret.) James Watkins has become a recognized national spokesman for ocean affairs.

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University of California, which foresaw the need to establish two new campuses in southern California.

FIG. 2. Gulf of California Expedition, 1939. (Left to Right) Erik Moberg, Roger Revelle, Seaman Andrew Boffinger, Richard Fleming (with binoculars), Machinist Bob MacDonald, George Hale, Lee Haines, Engineer Walter Robinson, Martin Johnson, and Loye H. Miller. [Reproduced with the permission of the SIO Archives, UCSD.] Roger had in mind a major university in the manner of The John Hopkins University or the University of Chicago, with a heavy concentration of graduate students. The plan ran into opposition by a 1956 University of California at Los Angeles (UCLA) review committee, which proposed that UCSD should be permitted to offer only lower division undergraduate courses at first, and only after a later review to add upper division courses, but not a graduate program. We pointed out that Scripps had been granting Ph.D. degrees when UCLA was still a teacher's college.

FIG. 3. MOHOLE project, aboard the CUSS I off Guadalupe Island in 1961. (Left to Right) John Steinbeck, Josh Tracey, Unidentified, William Riedel, Roger Revelle, Walter Munk, Gustav Arrhenius, and Willard Bascom, examining specimen. Photograph by Fritz Goro, Life Magazine (© Time Inc.).

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Roger (9) roasted them for trying to forestall competition: The Committees on Educational Policy . . . were experts at seeing clouds no bigger than a man's hand. It was clear to them that a new graduate school would draw money away from their own campuses; it might even attract outstanding scientists. . . . They thought it would be nice to have an undergraduate school at La Jolla, managed by a farm team of dedicated teachers, which could provide well-trained new graduate students for their own laboratories. Roger put in an enormous effort in recruiting faculty for his new school, originally housed on the Scripps Campus; among the recruits were Harold Urey, Joseph and Maria Mayer, Jim Arnold, David Bonner, Walter Elsasser, Martin Kamen, Bernd Matthias, and Bruno Zimm. The secret of Roger's recruiting success was not a secret at all. He put in a major effort to learn what these people really wanted to do and then went out to provide the opportunity for them to live their dream. But he was not unwilling to exercise some salesmanship. Judith and I were on the recruiting route, and Roger would end up at our home with an exhausted candidate in tow at cocktail time, saying, “And here is a typical faculty house.” There was at the time an unspoken covenant among La Jolla Realtors not to sell to Jews. Roger went out to break this covenant, realizing that it was incompatible with his vision of the university. He was somewhat aided by the fact that most members of the real estate community were not fundamentally opposed to enhancing their commissions. The chairman of the University of California Board of Regents at the time was the oil magnate Edwin Pauley. Pauley wanted the campus in Balboa Park in downtown San Diego. Roger wanted it next to Scripps. Regent Pauley had commissioned a study that concluded that the aircraft noise associated with Miramar Naval Air Station would make the site 20% more expensive than that at Balboa Park. Roger had gotten hold of a previous report by that same architect dealing with the location of Scripps Hospital (under the same flight pattern and even closer to the Air Station) which concluded that the noise would not appreciably increase the cost! Roger won that battle, but as it happened to King Pyrrhus of Epirus, he had won one too many. In 1961, when it came time to appoint the first chancellor, the Regents selected Herbert York. It was a major blow to Roger, reminiscent of the long delays in his appointment as Scripps Director. The Exile Roger determined that his continued presence on the campus would make it very difficult for Herbert York to function effectively, so he left for what turned out to be a 14-year exile. President Kerr appointed Roger to the meaningless position as Dean of Research for the University of California statewide. Roger next became Science Advisor to Secretary of Interior Morris Udall and then was appointed Richard Saltonstall Professor of Population Policy at Harvard University, a chair he held for just over a decade. Among his students was Benazir Bhutto and Albert Gore. Gore credited Roger with having aroused his interest in environmental problems. Many years later, during the 1992 presidential campaign, Gore was accused of having misrepresented Roger's position on global warming. The problem arose in connection with an article first published in the Cosmos Club Journal, “What to Do About Greenhouse Warming: Look Before You Leap.” The cautionary admonition “look before you leap” is uncharacteristically tame for Roger, and it is my contention that it represented more the views of the other authors, Fred Singer and Chauncey Starr. I cannot do justice to the many accomplishments during the exile era, but I need to mention one activity which goes back a long time: Roger's continuing love affair with India. Roger took many trips to India and served as an advisor to various government agencies on a broad range of topics, centered on food and population problems. I was amazed on a recent trip to learn of how many Indian careers and lives had been influenced by Roger.

FIG. 4. Revelle explaining core sample to roughneck aboard CUSS I in 1961. This is my favorite photograph of Roger; it shows his total attention to the person with whom he is speaking at the moment. Photograph by Fritz Goro, Life Magazine (© Time Inc.). Roger and Ellen thought of their Harvard years as some of the most fulfilling of their lives. Calling it an “exile” reflects my own provincial Scripps perspective. Coming Home In 1975 Roger returned to UCSD to become Professor of Science and Public Policy. For the next 15 years he taught courses in marine policy and population, and he continued to be active in oceanographic affairs. When in 1978 the American Association for the Advancement of Science (AAAS) decided to focus its international efforts on a few selected issues, Roger chaired the AAAS group that identified the build-up of heat-absorbing gases in the atmosphere as one such issue. As a result, the AAAS Board created the Committee on Climate, and Roger served as its chairman for a decade. The Committee was responsible for the first effort to identify the costs and benefits of increased atmospheric carbon dioxide. He received the National Medal of Science from President George Bush in 1991 for his pioneering work in the areas of carbon dioxide and climate modifications, oceanographic exploration presaging plate tectonics, and the biological effects of radiation in the marine environment, and studies of population growth and global food supplies. To a reporter asking why he got the medal, Roger (10) said, “I got it for being the grandfather of the greenhouse effect.” It is difficult to do justice to a man with such broad accomplishments. When questioned about his profession, Roger would reply “I am an oceanographer.” But this was hardly restrictive because he defined the profession of oceanography as whatever anyone at Scripps does. This has saved me on one occasion. During one of the chronic Scripps space

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shortages, Director William Nierenberg surprised Judith and me in a SIO laboratory as we were using laser pulses to remove encrustation's from a renaissance statue. “What are you doing?” Bill asked. “I am doing oceanography,” I replied.

FIG. 5. Roger in 1976. Photo by Glasheen. [Negative AN24/41906/484/34, UCSD Special Collections.] A Personal Appreciation Roger and I have collaborated on a number of papers: on a global compilation of the seasonal change in sea level, on an attempt to infer the melting of the Greenland ice cap from the slowing of the Earth's rate of rotation and the motion of the pole toward Greenland, and on a 1977 National Academy of Sciences report (11) in which we traced the partition CO2 among the atmosphere, ocean, and biosphere. Roger's way of working was anything but analytical; rather he followed a Sherlock Holmes procedure of eliminating one hypothesis after another. In doing his sums, he showed an accountant's revulsion for dropping nonsignificant digits. But my thoughts of Roger are not particularly related to these joint publications. He was my friend for 50 years. I remember weekends in the Revelle cottage in Julian, and sailing in the Aegean. I remember all-night sessions of Roger and Harry Hess at the Cosmos Club. I remember 9 months in the South Pacific, with a luncheon hosted by the Crown Prince, now King, of Tonga. I remember sleepless nights with Roger and John Steinbeck on the drilling ship CUSS I in Mexican waters prior to the demise of the MOHOLE Project. Toward the end of his life, Roger's health deteriorated; he walked in pain and with some difficulty. One year before his death, I was visiting John Knauss, then Administrator of The National Oceanographic and Atmospheric Administration (NOAA), to seek help for the Heard Island Expedition, when Roger unexpectedly showed up. He had walked the endless corridors of the commerce building to lend his silent support. During the expedition, when all the equipment was demolished in a gale on station in the South Indian Ocean, Roger sent a soothing message by fax: “Wish I were with you; and then I am glad I'm not.” Roger was upset by a critical news article on the Heard Island Expedition published in Science (14) and wrote a letter to the editor starting with the words: “Shame on you” (15). It was to be the last thing Roger published (Fig. 5). In an obituary for the Independent of London (12), the oceanographer Henry Charnock spoke for many of us when he noted that, “[f] or an informed view on earth science, and on its repercussions on the human predicament, he was in a class of his own.” Deborah Day at Scripps Archives is responsible for much of this material. 1. Revelle, R. (1956) The Biological Effects of Atomic Radiation: A Report to the Public (National Academy of Sciences, Washington, DC). 2. Sverdrup, H., Director of Scripps Institution of Oceanography. Letter to Comdr. Roger Revelle, Cosmos Club, Washington, DC, September 25, 1947. Roger Revelle Papers (MC 6), Box 2, Folder 10. SIO Archives, UCSD. 3. Revelle, R. Letter to Dean M. P. O'Brien, University of California, Berkeley, November 7, 1947. Roger Revelle Papers (MC 6), Box 2, Folder 10. SIO Archives, UCSD. 4. Fox, D., Hubbs, C., McEwen, G., Shepard, F. & ZoBell, C. Letter to Robert Sproul, President of the University of California, Office of the President, Berkeley, April 12, 1950. S. V. “Scripps Institution of Oceanography. Part I: Directorship 1947–50.” Bancroft Library, University Archives, University of California, Berkeley. 5. Revelle, R. & Suess, H. E. (1957) Tellus 9, 18–27. 6. Revelle, R., Broecker, W., Craig, H., Keeling, C. D. & Smagorinsky, J. (1965) Restoring the Quality of our Environment: Report of the Environmental Pollution Panel, President's Science Advisory Committee (The White House, Washington, DC), pp. 111–133. 7. Revelle, R. (1982) Sci. Am. 247, 35–43. 8. Daddario, E. Q. “The Revelle Impact,” Transcription of a speech delivered at the Scripps Institution of Oceanography, March 10, 1984, p. 3. Accession 84–14. SIO Archives, UCSD. 9. Revelle, R. “On Starting a University,” Manuscript prepared but not published by Daedalus, 1974, p. 3. Roger Revelle Papers (MC6A), Box 158, Folder 19. SIO Archives, UCSD. 10. Lister, P., “Revelle Awarded National Medal of Science ‘90,” San Diego Daily Transcript, June 27, 1990, p. 1A. 11. Revelle, R. & Munk, W. H. (1977) Energy and Climate (National Academy of Sciences, Washington, DC), pp. 140–158. 12. Charnock, H., “Professor Roger Revelle,” The Independent (London), August 5, 1991. 13. Day, D. “Memorandum of Conversation with Dr. Francis P. Shepard, July 27, 1981. SIO Archives, UCSD. 14. Cohen, J. (1991) Science 252, 912. 15. Revelle, R. (1991) Science 253, 118.

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Proc. Natl. Acad. Sci. USA Vol. 94, pp. 8280–8283, August 1997 Colloquium Paper This paper was presented at a colloquium entitled “Carbon Dioxide and Climate Change,” organized by Charles D. Keeling, held November 13–15, 1995, at the National Academy of Sciences, Irvine, CA.

Equilibration of the terrestrial water, nitrogen, and carbon cycles

(climate/ecosystems/global change/nitrogen use efficiency/resource use efficiency) DAVID S. SCHIMEL*, B. H. BRASWELL* †, AND W. J. PARTON‡

© 1997 by The National Academy of Sciences 0027-8424/97/948280-4$2.00/0 PNAS is available online at http://www.pnas.org. ABSTRACT Recent advances in biologically based ecosystem models of the coupled terrestrial, hydrological, carbon, and nutrient cycles have provided new perspectives on the terrestrial biosphere's behavior globally, over a range of time scales. We used the terrestrial ecosystem model Century to examine relationships between carbon, nitrogen, and water dynamics. The model, run to a quasi-steady-state, shows strong correlations between carbon, water, and nitrogen fluxes that lead to equilibration of water/ energy and nitrogen limitation of net primary productivity. This occurs because as the water flux increases, the potentials for carbon uptake (photosynthesis), and inputs and losses of nitrogen, all increase. As the flux of carbon increases, the amount of nitrogen that can be captured into organic matter and then recycled also increases. Because most plant-available nitrogen is derived from internal recycling, this latter process is critical to sustaining high productivity in environments where water and energy are plentiful. At steady-state, water/energy and nitrogen limitation “equilibrate,” but because the water, carbon, and nitrogen cycles have different response times, inclusion of nitrogen cycling into ecosystem models adds behavior at longer time scales than in purely biophysical models. The tight correlations among nitrogen fluxes with evapotranspiration implies that either climate change or changes to nitrogen inputs (from fertilization or air pollution) will have large and long-lived effects on both productivity and nitrogen losses through hydrological and trace gas pathways. Comprehensive analyses of the role of ecosystems in the carbon cycle must consider mechanisms that arise from the interaction of the hydrological, carbon, and nutrient cycles in ecosystems. Global models of the terrestrial carbon cycle used in geochemical and assessment studies have generally lacked any serious representation of ecological processes or feedbacks and have been extrapolated into the future using a simple parameterization of the relationship between atmospheric CO2 and ecosystem carbon storage (1, 2). Biosphere models used to calculate surface water and energy exchanges in climate models commonly employ sophisticated representations of photosynthesis and respiration, but omit biogeochemical processes associated with the formation and turnover of organic matter (3, 4). Recently, process-based models for terrestrial biogeochemistry have been developed, based on theory linking climate, soil properties, and species- or growth form-specific traits to biogeochemical responses of plants and microorganisms. These models simulate the uptake and release of carbon in response to light, water, temperature, and nutrients (5, 6, 7, 8, 9 and 10). The roles of climate and nutrient limitations inherent in modern ecology (discussed in refs. 11 and 12) are important because the sensitivity of ecosystem models to climate change and increasing CO2 is strongly modulated by nutrients (13, 14). Response of modeled carbon storage to increasing CO2 and temperature is modified by increasing nutrient limitation (14, 15). Large-scale patterns in terrestrial primary productivity, soil carbon, and soil metabolism can often be explained from simple equations using climate parameters (precipitation, actual evapotranspiration, solar radiation) (16, 17, 18, 19, 20, 21 and 22). However, nutrients often limit terrestrial primary productivity in the sense that added nutrients lead to additional plant growth and carbon storage (15, 23). Current process-level models couple biophysical and biogeochemical limits to ecosystem processes explicitly (14, 24, 25). Recent work suggests that, in fact, biophysical and biogeochemical (nutrient) limitations to productivity and carbon storage may come into equilibrium with each other as ecosystems develop over time (24, 25). In this paper, we present a model-based analysis of the processes whereby water/energy and biogeochemical controls over ecosystem productivity and carbon storage converge, as a theoretical underpinning for the eventual quantitative analysis of terrestrial biogeochemical response to global change. Model and Methods In this study, we used the Century terrestrial ecosystem model, developed by Parton et al. (26) over the past decade. In the past few years the model has been extensively evaluated relative to observations along climate gradients (25, 27), at continental scales (25), globally (13, 28), and compared with remote sensing (12, 25). The model simulates the major pathways for water, carbon, and nitrogen exchange, including atmospheric and biological N inputs, and gaseous, combustion-related, and hydrological N losses (12, 13, 26, 28, 29, 30 and 31). Century explicitly partitions live biomass and organic matter (nonliving) into compartments defined by differing turnover times. For the live components, these correspond to leaves, fine roots, coarse roots, branches, and stems. For organic matter the model is based on isotopic and other evidence for multiple turnover times in detritus and soil organic matter (28, 32, 33). The model is integrated globally using gridded global climate, soils, and vegetation data sets with 0.5 degree resolution (24). Results (annual fluxes) shown in this paper are from a simulation of the Northern Hemisphere, using an updated version of Century (24). For this analysis the model was integrated using CO2 concentrations and nitrogen input rates deemed to be representative of the preindustrial biosphere. For example, nitrogen inputs from precipitation were simulated to be 30–50% lower than current levels in moderately to severely polluted areas (34). We did this to simulate, for diagnostic purposes, a nearly steady-state biosphere. Much recent evidence suggests

*National Center for Atmospheric Research, P.O. Box 3000, Boulder, CO 80307-3000; †Institute for Earth, Oceans and Space, University of New Hampshire, Durham, NH 03824; and ‡Natural Resource Ecology Laboratory, Colorado State University, Fort Collins CO 80523

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that the forcing due to increasing N deposition and frequency of ecosystem disturbance over the past 50–100 years may have resulted in non-steady-state N cycles in much of the world (34, 35 and 36). Abbreviations: ET, evapotranspiration; NPP, net primary productivity. Equilibration of Nitrogen and Water Limitations In ref. 24 we argued that spatial patterns of biophysical and nitrogen limitation are correlated because carbon and nitrogen fluxes are both strongly influenced by water and energy availability. This mechanism of equilibration is evident in Century because the model simulates the inputs and losses of N, rather than being calibrated to observed ecosystem N stocks (25). The equations in Century governing nitrogen fluxes include biophysical and soil biogeochemical processes. Atmospheric inputs of N are directly linked to precipitation (wet deposition). Biological nitrogen fixation is influenced by soil N and C availability and is assumed to be correlated with annual evapotranspiration (ET). The correlation is based on information indicating high rates of N fixation in humid tropical and temperate rain forests, and generally lower rates in mesic and arid systems, although the biogeography of nitrogen fixation is poorly known (23). It is noteworthy that, globally, patterns of N inputs through all processes are poorly known, and given their importance, require much more study (37). N inputs, as expected (summing biological and atmospheric processes) are strongly correlated with annual ET (Table 1). Losses of nitrogen are controlled by soil moisture and water flux. Leaching losses of NO3 and dissolved organic N (DON) are directly controlled by the product of water flux and NO3/DON concentrations (28). Losses of N trace gases are linked to the rate of mineralization of NH4 and NO3 from organic matter, a rate that increases as temperature and soil moisture increase (28, 38). The proportional as well as absolute losses of gaseous N from inorganic N also increase with increasing soil moisture (30). Century simulates several pathways of N trace gas losses: the summed losses of N2, N2O, and NO from soil nitrification and denitrification are likewise highly correlated with ET (Table 1). This arises because of the strong first-order kinetic regulation of trace gas emissions with respect to soil inorganic N turnover. A key index of soil inorganic N turnover, N mineralization, is likewise strongly correlated with ET (Table 1). As noted in ref. 24, the correlation of N mineralization and ET, though strong, varies among ecosystem types, as is evident for other processes (see Fig. 2). Trace gas losses show similar patterns (data not shown), indicating ecosystem type-specific relationships between biophysical controls and N trace gas emissions, a factor not widely recognized (24). Spatial patterns of nitrate N leaching (data not shown) show strong dependence on ecosystem type, with many systems showing no or low losses; here we computed correlations for systems with non-zero leaching losses. Leaching losses are less directly related to ET, perhaps because ET is a poor predictor of available water below the rooting zone. Nitrate leaching is, however, strongly correlated with precipitation minus ET (P-E), which is related to the amount of water available for movement below the rooting zone (Table 1). Organic N leaching only occurs in a small fraction of grid cells (
10%) and generally at low rates. It is poorly correlated with either ET or P-E (Table 1). The low leaching losses of N from many of the world's ecosystems in this simulation of a preindustrial biosphere are consistent with Hedin et al. (35), who suggested that undisturbed ecosystems may have very low losses compared with the bulk of extant ecosystems. The results indicate significant correlation between key fluxes in the nitrogen budget and biophysical controls, although ecosystem-specific processes such as organic N leaching add some variability to patterns of equilibration. Table 1. Correlation structure emerging from key linkages between mechanisms shown in Fig. 1, as implemented in the simulation described in Model and Methods NMIN NPP NINPUT NGAS NO3 DON NMIN — 0.90 0.54 — — ET 0.67 0.71 0.96 0.71 0.33 0.00 P-E — — — 0.74 0.05 — — 0.74 — — NINPUT NMIN, nitrogen mineralization; NPP, net primary productivity; NINPUTs, nitrogen inputs; NGAS, trace gas losses of N; NO3, nitrate leaching; DON, organic nitrogen leaching; ET, evapotranspiration; P-E, precipitation minus ET. All correlations shown are significant at P < 0.05 (except for ET vs. DON).

In Century the potential for carbon fixation increases as evapotranspiration increases via an equation that constrains primary production based on moisture available for transpiration (28). This equation integrates precipitation, energy, and soil hydrological constraints over the water flux in evapotranspiration. ET is linked to both precipitation, soil properties and radiation, as radiant energy is the driving force for ET. Thus, ET, which together with soil hydrological properties, controls the partitioning of soil moisture into runoff and fluxes back to the atmosphere or to depths below the rooting zone. Primary production also requires nitrogen to form organic matter meeting critical C/N ratios for wood, foliage, and roots. On an annual time scale most plant-available N is derived from nitrogen mineralization, which arises from organic matter turnover (decomposition); rates of N mineralization range from 0.2 to 30 g·m2·yr−1, greatly exceeding inputs in most cases. N inputs range from 0.5 to 1.5 g·m2·yr−1. Whereas N availability can vary substantially from year to year, the natural nitrogen budget changes on centennial time scales, as inputs and losses are small fractions of soil N stocks, which typically exceed 500 g·m2. As a consequence of the tight coupling of the water/energy fluxes and nitrogen budget in Century, strong correlations between ET, nitrogen availability, and net primary productivity appear in global Century simulations (see Fig. 2). The correlations arise because water and energy fluxes controls both carbon and nitrogen fluxes (Fig. 1). These fluxes of carbon and nitrogen are mutually interdependent through the dual requirements of nitrogen in the formation of organic matter and of the role of organic matter decomposition in nitrogen mineralization. As water flux increases, N flux increases (inputs and losses), and likewise, the potential for carbon fixation increases. As carbon fixation increases, the amount of the N flux that can be captured in organic matter increases. As more nitrogen is captured in organic matter, its subsequent turnover also contributes to plant available N, allowing more plant productivity. Thus, water/energy and nutrient limitation of plant primary productivity and ecosystem carbon storage tend to “equilibrate” in near-steady-state ecosystems, as illustrated by the spatial patterns of correlation in Fig. 2. The relationships of NPP and N availability with ET are modulated by other factors that influence turnover times. The relationships between NPP, ET, and N are modified by ecosystem type-specific factors that control resource use efficiencies. Effectively these are the carbon-to-nutrient stoichiometry of plants and microorganisms, and water use efficiency (or organic matter produced per unit water transpired) (Fig. 2). Ecosystems with wider C/N ratios in plant tissue have higher NPP per unit N mineralization (higher nitrogen use efficiencies). Systems with lower C/N ratios in leaf and root tissues have higher rates of N cycling per unit ET. C/N ratios reflect both plasticity in foliar and root composition, and more significantly, changes in allocation between high and low-N tissues (wood vs. leaves or roots). Although large-scale patterns arise from system-level interactions of the biogeochemical and hydrological cycles, substantial variation is induced by

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species- and growth form-specific traits related to allocation patterns and C/N ratios. The correlation of variables in Fig. 2 indicates the extent to which NPP and nitrogen cycling are controlled by system-level dynamics: the vertical scatter indicates roughly the extent to which system-specific ecological traits influence NPP and nitrogen cycling.

FIG. 1. Schematic illustration of the coupling of water, nitrogen cycling, and carbon in ecosystems. Principle features of these coupled controls are that (i) water controls the inputs and outputs of nitrogen, (ii) increasing net primary productivity (NPP) allows more of the N flux through the system to be captured into organic matter, (iii) increasing organic N stocks allow for more N mineralization, supporting more NPP, and (iv) increasing precipitation both allows more NPP and more N cycling, thus water and nutrient limitation of NPP tend to become correlated. The model results are consistent with observations of large-scale correlations of NPP with direct or derived climate variables, but also with experimental evidence of nutrient limitation. The modulation of the water-carbon-nitrogen system by species- and/or growth formspecific traits implies that large-scale dynamics are influenced by population dynamics on time scales longer than the life spans of individual plants (years-centuries). The relationship of biogeochemistry to population dynamics is outside the scope of this paper, but see refs. 39 and 40. Conclusions We hypothesized that water and nitrogen limitations of NPP are correlated at steady-state because of the control of carbon and nitrogen fluxes by the water budget. We further hypothesized that these correlations arise because of the system-level structure of interactions among the water, carbon, and nitrogen cycles. In model simulations, the correlations between biophysical and nutrient limitations to NPP and carbon storage arise because both carbon and nitrogen fluxes (ecosystem inputs and outputs) are influenced by water and energy availability. This model-based analysis is consistent with the widespread reports of strong correlations of climate with ecosystem processes, suggesting dominant climate controls, and strong experimental evidence that nutrient additions can increase productivity and carbon storage. The tight correlations among N budgetary fluxes (Table 1) suggest that atmospheric trace gas composition may be affected by changes to either climate or N inputs via air pollution or fertilization. Predicted ecosystem behavior becomes more complex when biophysical and nutrient constraints are considered together as compared with purely biophysical formulations (24, 41, 42). The biophysical effects of temperature, moisture, and radiation on photosynthesis, plant respiration, and evapotranspiration can be simulated with relatively few ecosystem-specific controls (4). Nutrient cycling is additionally coupled to spatial patterns of N inputs (34, 35 and 36) and to patterns of plant allocation of carbon and nitrogen among roots, wood, and leaves. These allocation patterns, in turn, influence the distribution among long and short-lived compartments of living (e.g., wood vs. leaves) and detrital organic matter. As more of a system's organic matter becomes tied up in long-lived compartments, fewer nutrients are available for rapid recycling, and nutrient limitation becomes tied to processes with longer time scales, such as soil carbon turnover or tree mortality and wood decomposition.

FIG. 2. Results from an integration of Century for the Northern Hemisphere. Simulations used standard global climate, soils, and vegetation type distribution data sets and were carried out globally on an 0.5 × 0.5 degree grid. Points indicated in green are for forest ecosystems, yellow indicates grasslands, and black indicates “mixed” ecosystems that include both grasses and trees or shrubs (such as savannas). (a) The relationship between ET and NPP (r2 = 0.71). (b) The relationship between nitrogen mineralization and NPP (r2 = 0.90). Nutrient-mediated processes assume increasing importance as ecosystem behavior is considered on interannual and longer time scales because they can cause lagged responses to climate change and variability (24). Models such as those discussed by Sellers et al. (3) describe the behavior of the “fast” carbon-water-energy system (43); biogeochemical models add the consequences of slower processes such as soil carbon and biomass accumulation, and allocation patterns between leaves, roots, and wood. Whereas even biophysical models may have “memory” over one to two years through soil moisture storage, biogeochemical models can simulate lagged effects over de

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cades through the decomposition of wood or soil organic matter. Here we identify “equilibration” of the nitrogen budget with water/energy and carbon fluxes as an additional process causing decadal and longer time scale behavior. Just as perturbations to the climate system can cause the nitrogen and carbon systems to respond (4, 24), perturbations of the N inputs from air pollution or fertilization will also cause long-lived ecosystem changes (34, 36, 44). Analyses of the past interannual variability of the carbon cycle, and of its potential future behavior, must consider mechanisms that act through the coupled water/energy, carbon, and nitrogen cycles. We acknowledge the assistance of Rebecca McKeown, Melannie Hartmann, and Hank Fisher with conducting and analyzing global Century runs, with special thanks to Becky for her exceptional effort in completing the global calculations for this paper. Dennis Ojima, Beth Holland, Alan Townsend, and Jason Neff all helped conceive of or design the model experiments. This research was supported by the National Aeronautics and Space Administration Earth Observing System Interdisciplinary Science Program, and by the National Center for Atmospheric Research. The National Center for Atmospheric Research is sponsored by the National Science Foundation. 1. Enting, I. G., Wigley, T.M.L. & Heimann, M. (1994) Future Emissions and Concentrations of Carbon Dioxide: Key Ocean/Atmosphere/Land Analyses (Division of Atmospheric Research, Commonwealth Scientific and Industrial Research Organization, Australia), Tech. Paper No. 31. 2. Siegenthaler, U. & Joos, F. (1992) Tellus B 44, 186–207. 3. Sellers, P. J., Bounoua, L., Collatz, G. J., Randall, D. A., Dazlich, D. A., Los, S. O., Berry, J. A., Fung, I., Tucker, C. J., Field, C. B. & Jensen, T. G. (1996) Science 271, 1402–1406. 4. Sellers, P. J., Dickinson, R. E., Randall, D. A., Betts, A. K., Hall, F. G., Berry, J. A., Collatz, G. J., Denning, A. S., Mooney, H. A., Nobre, C. A., Sato, N., Field, C. B. & Henderson-Sellers, A. (1997) Science 275, 502–509. 5. Farquhar, G. D., Von Caemmerer, S. & Berry, J. A. (1980) Planta 149, 78–90. 6. Melillo, J. M., Naiman, R. J., Aber, J. D. & Linkins, A. E. (1984) Bull. Mar. Sci. 35, 341–356. 7. Bloom, A. J., Chapin, F. S., III, & Mooney, H. A. (1985) Annu. Rev. Ecol. Syst. 16, 363–393. 8. Chapin, F. S., III, Bloom, A. J., Field, C. B. & Waring, R. H. (1987) BioScience 37, 49–57. 9. Nobel, P. S. (1991) Physicochemical and Environmental Plant Physiology (Academic, San Diego). 10. Running, S.W. & Nemani, R. R. (1991) Clim. Change 19, 349–368. 11. Schulze, E. D., De Vries, W., Hauhs, M., Rosén, K., Rasmussen, L., Tann, O.-C. & Nilsson, J. (1989) Water Air Soil Pollut. 48, 451–456. 12. Schimel, D. S., Kittel, T. G. F. & Parton, W. J. (1991) Tellus AB 43, 188–203. 13. Schimel, D. S., Braswell Jr., B. H., Holland, E. A., McKeown, R., Ojima, D. S., Painter, T. H., Parton, W.J. & Townsend, A. R. (1994) Global Biogeochem. Cycles 8, 279–293. 14. VEMAP Participants (1995) Global Biogeochem. Cycles 9, 407–438. 15. Schimel, D. S. (1995) Global Change Biol. 1, 77–91. 16. Leith, H. (1975) in Primary Productivity of the Biosphere, eds. Leith, H. & Whittaker, R. B. (Springer, New York), pp. 237–263. 17. Uchijima, Z. & Seino, H. (1985) J. Agric. Meteorol. 40, 43–352. 18. Sala, O. E., Parton, W. J., Joyce, L. A. & Lauenroth, W. K. (1988) Ecology 69, 40–45. 19. Potter, C. S., Randerson, J. T., Field, C. B., Matson, P. A., Vitousek, P. M., Mooney, H. A. & Klooster, S.A. (1993) Global Biogeochem. Cycles 7, 811–841. 20. Gifford, R. M. (1994) Aust. J. Plant Physiol. 21, 1–15. 21. Zak, D. R., Tilman, D., Parmenter, R. R., Rice, C. W., Fisher, F. M., Vose, J., Milchunas, D. & Martin, C. W. (1994) Ecology 75, 2333–2347. 22. Post, W. M., Pastor, J., Zinke, P. J. & Stangenberger, A. G. (1985) Nature (London) 317, 613–616. 23. Vitousek, P. 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POTENTIAL RESPONSES OF SOIL ORGANIC CARBON TO GLOBAL ENVIRONMENTAL CHANGE

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Proc. Natl. Acad. Sci. USA Vol. 94, pp. 8284–8291, August 1997 Colloquium Paper This paper was presented at a colloquium entitled “Carbon Dioxide and Climate Change,” organized by Charles D. Keeling, held November 13–15, 1995, at the National Academy of Sciences, Irvine, CA.

Potential responses of soil organic carbon to global environmental change SUSAN E. TRUMBORE Department of Earth System Science, University of California, Irvine, CA 92697–3100

© 1997 by The National Academy of Sciences 0027-8424/97/948284-8$2.00/0 PNAS is available online at http://www.pnas.org. ABSTRACT Recent improvements in our understanding of the dynamics of soil carbon have shown that 20–40% of the approximately 1,500 Pg of C stored as organic matter in the upper meter of soils has turnover times of centuries or less. This fastcycling organic matter is largely comprised of undecomposed plant material and hydrolyzable components associated with mineral surfaces. Turnover times of fast-cycling carbon vary with climate and vegetation, and range from