NATURE | VOL 413 | 11 OCTOBER 2001 | www.nature.com 591 review article Catastrophic shifts in ecosystems Marten Scheffer*, Steve Carpenter², Jonathan A. Foley³, Carl Folke§ & Brian Walkerk * Department of Aquatic Ecology and Water Quality Management, Wageningen University, PO Box 8080, NL-6700 DDWageningen, The Netherlands ² Center for Limnology, University of Wisconsin, 680 North Park Street, Madison, Wisconsin 53706, USA ³ Center for Sustainability and the Global Environment (SAGE), Institute for Environmental Studies, University of Wisconsin, 1225West Dayton Street, Madison, Wisconsin 53706, USA § Department of Systems Ecology and Centre for Research on Natural Resources and the Environment (CNM), Stockholm University, S-10691 Stockholm, Sweden k CSIRO Sustainable Ecosystems, GPO Box 284, Canberra, Australian Capital Territory 2601, Australia ............................................................................................................................................................................................................................................................................ All ecosystems are exposed to gradual changes in climate, nutrient loading, habitat fragmentation or biotic exploitation. Nature is usually assumed to respond to gradual change in a smooth way. However, studies on lakes, coral reefs, oceans, forests and arid lands have shown that smooth change can be interrupted by sudden drastic switches to a contrasting state. Although diverse events can trigger such shifts, recent studies show that a loss of resilience usually paves the way for a switch to an alternative state. This suggests that strategies for sustainable management of such ecosystems should focus on maintaining resilience. T he notion that ecosystems may switch abruptly to a contrasting alternative stable state emerged from work on theoretical models 1,2 . Although this provided an inspiring search image for ecologists, the ®rst experi- mental examples that were proposed were criticized strongly 3 . Indeed, it seemed easier to demonstrate shifts between alternative stable states in models than in the real world. In particular, unravelling the mechanisms governing the behaviour of spatially extensive ecosystems is notoriously dif®cult, because it requires the interfacing of phenomena that occur on very different scales of space, time and ecological organization 4 . Nonetheless, recent studies have provided a strong case for the existence of alternative stability domains in various important ecosystems 5±8 . Here, we do not address brief switches to alternative states such as described for pest outbreaks 9 . Also, we do not fully cover the extensive work on positive feedbacks and multiple stable states in ecological systems. Instead, we concentrate on observed large-scale shifts in major ecosystems and their explanations. After sketching the theoretical framework, we present an overview of results from different ecosystems, highlight emerging patterns, and discuss how these insights may contribute to improved management. Theoretical framework Ecosystem response to gradually changing conditions External conditions to ecosystems such as climate, inputs of nutrients or toxic chemicals, groundwater reduction, habitat fragmentation, harvest or loss of species diversity often change gradually, even linearly, with time 10,11 . The state of some ecosystems may respond in a smooth, continuous way to such trends (Fig. 1a). Others may be quite inert over certain ranges of conditions, responding more strongly when condi- tions approach a certain critical level (Fig. 1b). A crucially different situation arises when the ecosystem response curve is `folded' backwards (Fig. 1c). This implies that, for certain environmental conditions, the ecosystem has two alternative stable states, separated by an unstable equilibrium that marks the border between the `basins of attraction' of the states. The presence of alternative stable states has profound impli- cations for the response to environmental change (Fig. 2a). When the ecosystem is in a state on the upper branch of the folded curve, it can not pass to the lower branch smoothly. Instead, when conditions change suf®ciently to pass the thresh- old (`saddle-node' or `fold' bifurcation, F 2 ), a `catastrophic' transition to the lower branch occurs. Note that when one monitors the system on a stable branch before a switch, little change in its state is observed. Indeed, such catastrophic shifts occur typically quite unannounced, and `early-warning signals' of approaching catastrophic change are dif®cult to obtain. Another important feature is that to induce a switch back to the upper branch, it is not suf®cient to restore the environmental conditions of before the collapse (F 2 ). Instead, one needs to go back further, beyond the other switch point (F 1 ), where the system recovers by shifting back to the upper branch. This pattern, in which the forward and backward switches occur at different critical conditions, is known as hysteresis. The degree of hysteresis may vary strongly even in the same kind of ecosystem. For instance, shallow lakes can have a pronounced hysteresis in response to nutrient loading (Fig. 1c), whereas deeper lakes may react smoothly (Fig. 1b) 12 . A range of mathematical models of speci®c ecological systems with alter- native stable states has been published. Box 1 shows an example of a simple model that can be thought of as describing deserti®cation or lake eutrophication. Effects of stochastic events In the real world, conditions are never constant. Stochastic events such as weather extremes, ®res or pest outbreaks can cause ¯uctuations in the conditioning factors (horizontal axis) but often affect the state (vertical axis) directly, for example, by wiping out parts of populations. If there is only one basin of attraction, the system will settle back to essentially the same state after such events. However, if there are alternative stable states, a suf®ciently severe perturbation of the ecosystem state may bring the system into the basin of attraction of another state (Fig. 2b). The likelihood of this depends not only on the perturbation, but also on the size of the attraction basin. In terms of stability landscapes (Fig. 3), if the valley is small, a small perturbation may be enough to displace the ball far enough to push it over the hill, resulting in a shift to the alternative stable state. Following Holling 1 , we here use the term `resilience' to refer the size of the valley, or basin of attraction, around a state, which corresponds to the maximum perturbation that can be taken without causing a shift to an alternative stable state. In systems with multiple stable states, gradually changing conditions may have little effect on the state of the ecosystem, but nevertheless reduce the size of the attraction basin (Fig. 3). This loss of resilience makes the system more fragile in the sense that can easily be tipped into a contrasting state by stochastic events. Such stochastic ¯uctuations may often be driven externally; however, they can also result from internal system dynamics. The latter can happen if the alternative © 2001 Macmillan Magazines Ltd