Review

TRENDS in Ecology and Evolution

Vol.21 No.6 June 2006

Global change ecology

William H. Schlesinger
The Nicholas School of the Environment and Earth Sciences, Duke University, Durham, NC 27708, USA

Ecology has expanded from its traditional focus on organisms to include studies of the Earth as an integrated ecosystem. Aided by satellite technologies and computer models of the climate of the Earth, global change ecology now records basic parameters of our planet, including its net primary productivity, biogeochemical cycling and effects of humans on it. As I discuss here, this new perspective shows us what must be done to transform human behaviors to enable the persistence of life on Earth under human stewardship. Introduction When I was a graduate student during the early 1970s, ecology was about organisms. The prestigious places to publish were Ecology and The American Naturalist, and the focus was on the number of individuals or species found in nature, their rates of reproduction and the marvelous adaptations that enabled them to persist in their native habitats. The research was usually done at eld stations; each of us chose an idyllic place to spend the summer studying how nature is put together. Today, we see a huge emphasis on a broader view: what is the effect of life on Earth? What changes are we, as the dominant species on the planet, forcing on the habitats of all other species, and how are we affecting the future prospects for life on Earth? What can we do about our rapidly changing planet? All these questions comprise global change science, which lls the pages of an explosion of new journals that focus on the past and future of our planet. Early studies of Earth system function There were harbingers to the birth of this new discipline. During the late 1950s, Roger Revelle commented that humans were performing an unreplicated global experiment by raising the concentration of carbon dioxide (CO2) in our atmosphere with potentially serious, but unknown, consequences [1]. By 1960, working with Revelle, Dave Keeling [2] had shown that not only was the CO2 concentration increasing, but that one could also see a regular oscillation in its concentration that must be due to the photosynthesis of land plants in the temperate zone. My colleague Dan Livingstone once said that the graph made him feel as if I had just put my nger on the beating, living heart of the world [3]. During the 1960s, Gene Odum showed that one could trace the ow of energy through ecosystems, focusing not so much on the individual species, but on an attempt to understand the overall process by which the products of
Corresponding author: Schlesinger, W.H. (schlesin@duke.edu). Available online 23 March 2006

photosynthesis either move to higher trophic levels, such as humans, or are dissipated in the environment [4]. Herb Bormann and Gene Likens [5] did the same for the ow of material elements, such as calcium, potassium and other elements that anchor the biochemistry of all organisms. Ecologists scrambled to study primary production and nutrient cycling as part of the International Biological Program (IBP; http://www7.nationalacademies.org/ archives/International_Biological_Program.html). A milestone was reached when Robert Whittaker [6] and, working independently, Helmut Lieth [7] used these disparate eld studies to estimate the net primary production of the entire land surface of the Earth. They were the rst to show just how much photosynthesis the biosphere had to work with each year. Remarkably, using rather crude methods, they arrived at estimates (between 50 and 60 Pg C yrK1) that are similar to measurements from satellites today [8]. Most satellite estimates of plant productivity on Earth are based on the formulation of the Normalized Difference Vegetation Index (NDVI), developed by Compton Tucker and colleagues [9] and rst used to study changes in greenness from the Sahel of Africa [10] to high northern latitudes [11]. I mark the beginning of global change science with the publication of The Biosphere as a special issue of Scientic American in 1970. This was the rst time that I saw an integration of the science that viewed our planet as a closed ecosystem in which photosynthetic organisms captured sunlight energy, enabling a profusion of other forms of life. An array of articles outlined the global biogeochemical cycles and the emerging human impacts on them. Not without controversy and criticism, the publication of Limits to Growth in 1974 made many people realize how exponential growth in both population and economics would collide with the resources available on a nite plane [12]. Global views of human impacts Documentation of human impacts on the biosphere was not long in coming. In 1974, Mario Molina and Sherwood Rowland [13] predicted that chlorouorocarbons (CFCs) would destroy stratospheric ozone, a forecast that is conrmed dramatically in satellite photos from NASA of the ozone hole from the 1980s to today (Figure 1). This small human perturbation of the global chlorine cycle posed a real threat to the survival of life on Earth, or at least on the land surface [14]. Geochemists showed that the annual human production and mobilization of many important elements of the periodic table (especially nitrogen, phosphorus, sulfur and most metals of economic interest) rivaled that of nature [15]. In 1986, Peter

www.sciencedirect.com 0169-5347/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2006.03.004

Review

TRENDS in Ecology and Evolution

Vol.21 No.6 June 2006

349

the array of Earth Observing System (EOS) satellites that now monitor our planet, recording basic characteristics of its temperature, photosynthesis, atmospheric chemistry and land cover, all beamed down to receiving stations even as you read this (http://eospso.gsfc.nasa.gov/) [24]. Where we are today Through early global change science, we gained a broad perspective on the impact of humans on nature. There is little doubt that humans are now a major evolutionary force on Earth [25], and that our activities dominate its ecosystems, both on land and in the sea [26,27]. Satellite views of night-time lighting show the pervasive human presence on our planet [28,29]. Every ecosystem on Earth is now bathed in high CO2 from fossil fuel combustion. Chemicals of human origin are found on all continents [30] and are rapidly mixing to the deepest reaches of the sea [31]. Even the reection or albedo of the Earth, as seen by earthshine on the Moon, has increased as a result of a greater burden of atmospheric aerosols and clouds [32]. The pristine eld stations that we visited as graduate students are of little relevance to most of the surface of the Earth that is now managed by humans and under rapid degradation under our stewardship. What matters most for the organisms that we studied so diligently 30 years ago is not so much how they perform on Natures stage, but whether the stage will exist for them at all. Priorities for global change science: the sea There is much science left to do, especially on the 70% of the surface of the Earth that is covered by salt water. Although we have a fairly good estimate of the net primary production of the oceans [33], we have only a limited grasp of the sources of nitrogen, phosphorus, iron and silicon that fuel ocean productivity. New research on sources of nitrogen to the oceans and its loss via anaerobic ammoniaoxidizing bacteria has recently rewritten what we know about nitrogen cycling in the sea [34]. Increasing atmospheric CO2 levels have already lowered ocean pH by 0.1 and are likely to lead to much greater acidication during the rest of this century [35]. Climatic change has also raised the temperature of the oceans and lowered the salinity over broad regions [36,37]. We are also likely to change marine net primary productivity as we alter the provision of essential elements to marine ecosystems through the dispersal of soils by wind erosion [38]. There is every indication that we have overexploited the oceans. Nearly 8% of oceanic productivity goes to support the current harvest of protein from ocean waters [39]. Increasingly, we see signs that the oceans are not an innite sink in which to dilute the pollutants of industrialized society; yet we lack a good understanding of the sources of mercury, polybrominated organic compounds and other substances that might render oceanic sh unt for human consumption. Are we polluting the last large domain on Earth, or are some of these compounds natural [4042]? Do species matter? The original questions posed by NASA are ever more relevant today: How much nature must be left in its

Figure 1. Total column ozone as recorded by the TOMS satellite of NASA on 5 October 2005, one of the largest and deepest years on record for the loss of stratospheric ozone over Antarctica. Reproduced with permission from http:// jwocky.gsfc.nasa.gov/.

Vitousek and colleagues [16] estimated that humans use or dominate approximately 40% of the terrestrial net primary production on Earth [17,18], not a pretty picture for the future of most other species that share the planet with us. General circulation models and satellite measurements of the climate of the Earth conrmed what Svante Arrhenius [19] had predicted nearly a century earlier: increasing levels of CO2 in the atmosphere of the Earth, a perturbation of the global carbon cycle, would lead to a warmer planet, as seen today [20,21]. These empirical studies were enriched by theorists. During the 1960s, NASA sponsored a program of science to examine closed systems, with a desire to ascertain the minimum complexity that would be necessary for humans to survive in a spacecraft designed for long-distance explorations of the solar system [22]. Of course, then as now, the Earth has been our planetary spaceship. The 1979 publication of Gaia by James Lovelock [23] offered a provocative view that the biosphere on Earth was analogous to an organism, having emergent traits such as homeostasis that fostered its own persistence. Each species on Earth was thought to contribute in some small fashion to the stable conditions for life on Earth. Although Gaia has few followers now, the real impact of the book was that it made an entire generation of ecologists think broadly about planetary ecology. In 1969, NASA took us to the Moon, where we could look at our planet against the dark backdrop of space. In 1976, NASA took its technology to Mars, where it measured and photographed what we could expect on a planet without evidence of life. And, during the 1990s, NASA applied its technology to planet Earth, by launching
www.sciencedirect.com

100

125

150

175

200

Dobson units Dark gray < 100 and > 500 DU

225

250

275

300

325

350

375

400

425

450

475

500

350

Review

TRENDS in Ecology and Evolution

Vol.21 No.6 June 2006

natural state for sustainable Earth system function? Setting aside the ethics and aesthetics of preserving biodiversity, how simple can we make an ecosystem, while still seeing it function well without massive, articial human interventions, such as cultivation, irrigation, fertilization and pest control? Work by David Tilman et al. [43], which showed greater losses of nitrate beneath grassland ecosystems with depauperate species composition, links healthy ecosystem function to high species diversity. Does diversity beget stability or is there much redundancy of species that are pleasing to the eye but nonessential to the sustainability of a full planet? New questions also face us: What are the effects of the genetically modied organisms that enable us to supply new, articial species to nature, at the expense of the natural genetic diversity that is the raw material of evolution? What can we expect from our efforts, both purposeful and inadvertent, to homogenize the ora and fauna of the Earth as rapid and frequent travel and trade accompany our globalization of commerce and culture? How will we respond to disease pandemics? As we anticipate and adapt to changes in the climate and chemistry of the Earth, we need large-scale and longterm experiments to understand the response of biota to incremental CO2, nitrogen and ozone, and to changes in temperature and precipitation. Experiments using FreeAir CO2 Enrichment (FACE) in forests [44], iron additions to seawater [45] and 15N additions to streams [46] have done much to elucidate the response of whole ecosystems to human perturbations. The next phase of work should use factorial experiments so that we can understand how nature will respond to multiple stresses. Fortunately, we have wonderful new tools with which to do our science better. Molecular techniques will enable us to identify and understand the microbial communities that dominate so much of the biogeochemical cycling on Earth. For example, molecular systematics has been used to identify the bacteria catalyzing the anammox reaction converting NH4 to N2 in seawater [47]. Mass spectrometry to analyze the proportion of stable isotopes in different pools and uxes has revolutionized how we recognize the importance of biology in controlling the chemistry of Earth. Eddy covariance methods enable us to measure the net carbon exchange of large areas of the surface of the Earth (e.g. [48]) and remote-sensing technologies will enable us to monitor the function of ecosystems with much greater sample frequency in space and time than was ever before possible. These measurements are crucial if we are to build models of Earth system function that effectively couple surface processes to changes in climate and climatic forcings. Mercifully, each day, we see increases in our computational abilities to synthesize all the data. Beliefs and politics In some corners of the globe, policy makers and politicians pay close attention to the science that shows what will happen to a planet under inattentive stewardship. In much of the undeveloped world, however, the local population is perplexed about what to do to ensure a sustainable future when facing the immediate question of how to provide enough food and clean water to survive
www.sciencedirect.com

each day. Sadly, in other corners, concern is shallow; many of those who could afford to help believe that some type of divine intervention will carry us through a bottleneck of an exponentially rising human population and its increasing demand for resources on a nite planet [49]. They want no personal sacrice. Perhaps what we learned best from our early eld studies of ecology is that human behavior might not be far removed from that of other organisms. Each squirrel on my bird tray feeds as if tomorrow is simply another day. Many global change scientists talk of sustainability science. Indeed, there is heated debate about the reality and meaning of the phrase sustainable development. In the pre-industrial era, humans lived in concert with nature. No doubt it was a hard life, but it was sustained for centuries. The question we now face is whether we can live the way we aspire to today, without degrading the life support systems of the planet that would sustain us tomorrow. And now we must try our best simply to preserve the species that we studied so fervently just a few decades ago. Global change science has a big agenda before it and little time in which to do it.
References
1 Revelle, R. and Suess, H.E. (1957) Carbon dioxide exchange between the atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9, 1827 2 Keeling, C.D. (1960) The concentration and isotopic abundances of carbon dioxide in the atmosphere. Tellus 12, 200203 3 Livingstone, D.A. (1973) Summary and envoi. In Carbon and the Biosphere (Woodwell, G.M. and Pecan, E.V., eds), pp. 366368, National Technical Information Service 4 Odum, E.P. (1968) Energy ow in ecosystems: a historical review. Am. Zool. 8, 1118 5 Bormann, F.H. and Likens, G.E. (1967) Nutrient cycling. Science 155, 424429 6 Whittaker, R.H. (1970) Communities and Ecosystems, MacMillan 7 Lieth, H. (1975) Modeling the primary productivity of the world. In Primary Productivity of the Biosphere (Lieth, H. and Whittaker, R.H., eds), pp. 237263, Springer 8 Field, C.B. et al. (1998) Primary productivity of the biosphere: integrating terrestrial and oceanic components. Science 281, 237240 9 Tucker, C.J. and Sellers, P.J. (1986) Satellite remote sensing of primary production. Int. J. Remote Sens. 7, 13951416 10 Tucker, C.J. et al. (1990) Expansion and contraction of the Sahara desert from 1980 to 1990. Science 253, 299301 11 Myneni, R.B. et al. (1997) Increased plant growth in northern high latitudes from 1981 to 1991. Nature 386, 698702 12 Meadows, D.H. et al. (1974) The Limits to Growth, Universe Books 13 Molina, M.J. and Rowland, F.S. (1974) Stratospheric sink for chlorouoromethanes: chlorine atom-catalyzed destruction of ozone. Nature 249, 810812 14 Graedel, T.E. and Keene, W.C. (1995) Tropospheric budget of reactive chlorine. Global Biogeochem. Cycles 9, 4777 15 Bertine, K.K. and Goldberg, E.D. (1971) Fossil fuel combustion and the major sedimentary cycle. Science 173, 233235 16 Vitousek, P.M. et al. (1986) Human appropriation of the products of photosynthesis. Bioscience 36, 368373 17 Rojstaczer, S. et al. (2001) Human appropriation of photosynthesis products. Science 294, 25492552 18 Imhoff, M.L. et al. (2004) Global patterns in human consumption of net primary production. Nature 429, 870872 19 Arrhenius, S. (1896) On the inuence of carbonic acid in the air upon the temperature of the ground. Lond. Edin. Dub. Philos. Mag. J. Sci. 41, 237276 20 Harries, J.E. et al. (2001) Increases in greenhouse forcing inferred from the outgoing longwave radiation spectra of the Earth in 1970 and 1997. Nature 410, 355357

Review

TRENDS in Ecology and Evolution

Vol.21 No.6 June 2006

351

21 Hansen, J. et al. (2005) Earths energy imbalance: conrmation and implications. Science 308, 14311435 22 Taub, F.B. (1974) Closed ecological systems. Annu. Rev. Ecol. Syst. 5, 139160 23 Lovelock, J.E. (1979) Gaia, Oxford University Press 24 Running, S.W. et al. (2004) A continuous satellite-derived measure of global terrestrial primary production. Bioscience 54, 547560 25 Palumbi, S.R. (2001) Humans as the worlds greatest evolutionary force. Science 293, 17861790 26 Foley, J.A. et al. (2005) Global consequences of land use. Science 309, 570574 27 Vitousek, P.M. et al. (1997) Human domination of Earths ecosystems. Science 277, 494499 28 Elvidge, C.D. et al. (1997) Satellite inventory of human settlements using nocturnal radiation emissions: a contribution for the global toolchest. Glob. Change Biol. 3, 387395 29 Sanderson, E.W. et al. (2002) The human footprint and the last of the wild. Bioscience 52, 891904 30 Simonich, S.L. and Hites, R.A. (1995) Global distribution of persistent organochlorine compounds. Science 269, 18511854 31 Krysell, M. and Wallace, D.W.R. (1988) Arctic ocean ventilation studied with a suite of anthropogenic halocarbon tracers. Science 242, 746749 32 Palle, E. et al. (2004) Changes in Earths reectance over the past two decades. Science 304, 12991301 33 Behrenfeld, M.J. and Falkowski, P.G. (1997) Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 120 34 Arrigo, K.R. (2005) Marine microorganisms and global nutrient cycles. Nature 437, 349355 35 Orr, J.C. et al. (2005) Anthropogenic ocean acidication over the twenty-rst century and its impact on calcifying organisms. Nature 437, 681686

36 Dickson, B. et al. (2002) Rapid freshening of the deep North Atlantic Ocean over the past four decades. Nature 416, 832837 37 Levitus, S. et al. (2000) Warming of the world ocean. Science 287, 22252229 38 Jickells, T.D. et al. (2005) Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308, 6771 39 Pauly, D. and Christensen, V. (1995) Primary production required to sustain global sheries. Nature 374, 255257 40 Mason, R.P. et al. (1994) The biogeochemical cycling of elemental mercury: anthropogenic inuences. Geochim. Cosmochim. Acta 58, 31913198 41 Monteiro, L.R. and Furness, R.W. (1997) Accelerated increase in mercury contamination in North Atlantic mesopelagic food chains as indicated by time series of seabird feathers. Environ. Toxicol. Chem. 16, 24892493 42 Teuten, E.L. et al. (2005) Two abundant bioaccumulated halogenated compounds are natural products. Science 307, 917920 43 Tilman, D. et al. (1996) Productivity and sustainability inuenced by biodiversity in grassland ecosystems. Nature 379, 718720 44 Norby, R.J. et al. (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc. Natl. Acad. Sci. U. S. A. 102, 1805218056 45 Coale, K.H. et al. (2004) Southern ocean iron enrichment experiment: carbon cycling in high- and low-Si waters. Science 304, 408414 46 Mulholland, P.J. et al. (2004) Stream denitrication and total nitrate uptake rates measured using a eld 15N tracer addition approach. Limnol. Oceanogr. 49, 809820 47 Kuypers, M.M.M. et al. (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608611 48 Ciais, P. et al. (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529533 49 Wackernagel, N. et al. (2002) Tracking the ecological overshoot of the human economy. Proc. Natl. Acad. Sci. U. S. A. 99, 92669271

Have you contributed to an Elsevier publication?

Did you know that you are entitled to a 30% discount on books?
A 30% discount is available to ALL Elsevier book and journal contributors when ordering books or stand-alone CD-ROMs directly from us. To take advantage of your discount: 1. Choose your book(s) from www.elsevier.com or www.books.elsevier.com 2. Place your order Americas: TEL: +1 800 782 4927 for US customers TEL: +1 800 460 3110 for Canada, South & Central America customers FAX: +1 314 453 4898 E-MAIL: author.contributor@elsevier.com All other countries: TEL: +44 1865 474 010 FAX: +44 1865 474 011 E-MAIL: directorders@elsevier.com Youll need to provide the name of the Elsevier book or journal to which you have contributed. Shipping is FREE on pre-paid orders within the US, Canada, and the UK. If you are faxing your order, please enclose a copy of this page. 3. Make your payment This discount is only available on prepaid orders. Please note that this offer does not apply to multi-volume reference works or Elsevier Health Sciences products.

For more information, visit www.books.elsevier.com

www.sciencedirect.com