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Trophic Downgrading of Planet Earth James A Trophic Downgrading of Planet Earth James A. Estes, et al. Science 333, 301 (2011); DOI: 10.1126/science.1205106 This copy is for your personal, non-commercial use only. If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this infomation is current as of July 14, 2011 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/333/6040/301.full.html Supporting Online Material can be found at: http://www.sciencemag.org/content/suppl/2011/07/13/333.6040.301.DC1.html on July 15, 2011 This article cites 63 articles, 11 of which can be accessed free: http://www.sciencemag.org/content/333/6040/301.full.html#ref-list-1 This article appears in the following subject collections: Ecology http://www.sciencemag.org/cgi/collection/ecology www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2011 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. REVIEW Alternative stable states occur when perturbations of sufficient magnitude and direction push ecosys- tems from one basin of attraction to another (12). Trophic Downgrading of Planet Earth Tipping points (also known as thresholds or break- points), around which abrupt changes in ecosystem James A. Estes,1* John Terborgh,2 Justin S. Brashares,3 Mary E. Power,4 Joel Berger,5 structure and function (a.k.a. phase shifts) occur, William J. Bond,6 Stephen R. Carpenter,7 Timothy E. Essington,8 Robert D. Holt,9 often characterize transitions between alternative Jeremy B. C. Jackson,10 Robert J. Marquis,11 Lauri Oksanen,12 Tarja Oksanen,13 stable states. Ecosystem phase shifts can also dis- Robert T. Paine,14 Ellen K. Pikitch,15 William J. Ripple,16 Stuart A. Sandin,10 Marten Scheffer,17 play hysteresis, a phenomenon in which the loca- Thomas W. Schoener,18 Jonathan B. Shurin,19 Anthony R. E. Sinclair,20 Michael E. Soulé,21 tions of tipping points between states differ with Risto Virtanen,22 David A. Wardle23 the directionality of change (13). A third key con- cept, connectivity, holds that ecosystems are built Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. around interaction webs within which every spe- The loss of these animals may be humankind’s most pervasive influence on nature. Although such cies potentially can influence many other species. losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading Such interactions, which include both biological effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This processes (e.g., predation, competition, and mutu- empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also alism) and physicochemical processes (e.g., the highlights the unanticipated impacts of trophic cascadesonprocessesasdiverseasthedynamicsof nourishing or limiting influences of water, temper- disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings ature, and nutrients), link species together at an emphasize the urgent need for interdisciplinary researchtoforecasttheeffectsoftrophicdowngrading array of spatial scales (from millimeters to thou- on process, function, and resilience in global ecosystems. sands of kilometers) in a highly complex network. Taken together, these relatively simple concepts he history of life on Earth is punc- set the stage for the idea of trophic downgrading. tuated by several mass extinction events (2), during which global T 1 on July 15, 2011 biological diversity was sharply reduced. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA. 2Center for Tropical These events were followed by novel Conservation, Nicholas School of the Environment and Earth changes in the evolution of surviving Sciences, Post Office Box 90381, Duke University, Durham, NC species and the structure and function of 27708, USA. 3Department of Environmental Science, Policy, their ecosystems. Our planet is presently and Management, University of California, Berkeley, CA 94720, USA. 4Department of Integrative Biology, Valley Life Sciences in the early to middle stages of a sixth Building, University of California, Berkeley, CA 94720, USA. mass extinction (3), which, like those be- 5Division of Biological Sciences, University of Montana, fore it, will separate evolutionary winners Missoula, MT 59812, USA and Wildlife Conservation Society, 6 from losers. However, this event differs Bozeman, MT 59715, USA. Botany Department, University of Cape Town, Private Bag, Rondebosch 7701, South Africa. www.sciencemag.org from those that preceded it in two fun- 7Center for Limnology, 680 North Park Street, University of damental ways: (i) Modern extinctions are largely so doing, we demonstrate the influence of predation Wisconsin, Madison, WI 53706, USA. 8School of Aquatic and being caused by a single species, Homo sapiens, and herbivory across global ecosystems and bring Fishery Sciences, University of Washington, Box 355020, and (ii) from its onset in the late Pleistocene, the to light the far-reaching impacts of trophic down- Seattle, WA 98195, USA. 9Department of Biology, Post Office sixth mass extinction has been characterized by grading on the structure and dynamics of these Box 118525, University of Florida, Gainesville, FL 32611, USA. 10Center for Marine Biodiversity and Conservation, Scripps the loss of larger-bodied animals in general and of systems. These findings suggest that trophic down- Institution of Oceanography, 9500 Gilman Drive, La Jolla, CA apex consumers in particular (4, 5). grading acts additively and synergistically with other 92093, USA. 11Department of Biology, University of Missouri– St. Louis, One University Boulevard, St. Louis, MO 63121, USA. The loss of apex consumers is arguably human- anthropogenic impacts on nature, such as climate Downloaded from 12 kind’s most pervasive influence on the natural and land use change, habitat loss, and pollution. Department of Biology, Section of Ecology, University of Turku, FI-20014 Turku, Finland and Department of Natural world. This is true in part because it has occurred Sciences, Finnmark University College, N-9509 Alta, Norway. globally and in part because extinctions are by their Foundations in Theory 13Department of Biology, Section of Ecology, University of very nature perpetual, whereas most other envi- Ecological theory has long predicted that major Turku, FI-20014 Turku, Finland and Department of Ecology and ronmental impacts are potentially reversible on shifts in ecosystems can follow changes in the Environmental Science, Umeå University, SE-90087 Umeå, Sweden. 14Department of Biology, Box 351800, University of decadal to millenial time scales. Recent research abundance and distribution of apex consumers Washington, Seattle, WA 98195, USA. 15School of Marine and suggests that the disappearance of these animals (9, 10). Three key elements of that theory provide Atmospheric Sciences, Stony Brook University, Stony Brook, NY reverberates further than previously anticipated the foundation for interpreting recurrent patterns 11794, USA. 16Department of Forest Ecosystems and Society, (6–8), with far-reaching effects on processes as suggestive of trophic downgrading in more re- 314 Richardson Hall, Oregon State University, Corvallis, OR 97331, USA. 17Aquatic Ecology and Water Quality Management diverse as the dynamics of disease; fire; carbon cent empirical work across ecosystems. First is the Group, Department of Environmental Sciences, Wageningen sequestration; invasive species; and biogeochem- idea that an ecosystem may be shaped by apex University, Post Office Box 8080, 6700 DD Wageningen, ical exchanges among Earth’s soil, water, and consumers, which dates back more than a century Netherlands. 18Section of Evolution andEcologyandCenterfor Population Biology, 6328 Storer Hall, University of California, atmosphere. but was popularized in the 1960s (9). This concept 19 Here, we review contemporary findings on the was later formalized as the dynamic notion of Davis, CA 95616, USA. Department of Zoology, University of “ ” British Columbia, 6270 University Boulevard, Vancouver, BC V6T consequences of removing large apex consumers trophic cascades, broadly defined as the propa- 1Z4, Canada. 20Centre for Biodiversity Research, 6270 University from nature—a process we refer to as trophic down- gation of impacts by consumers on their prey down- Boulevard, University of British Columbia, Vancouver, BC V6T grading. Specifically, we highlight the ecological ward through food webs (11). Theoretical work 1Z4, Canada. 21Post Office Box 1808, Paonia, CO 81428, USA. 22Department of Biology, University of Oulu, FI-90014 Oulu, theory that predicts trophic downgrading, consider on factors that control ecosystem state resulted 23 “ Finland. Department of Forest Ecology and Management,
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