P1: FXY September 15, 2000 20:11 Annual Reviews AR113.18 RESILIENCE-THEORY AND PRACTICE 427 measures for resilience are near equilibrium ones���such as characteristic return time as defined above. The concept of ecological resilience presumes the existence of multiple stability domains and the tolerance of the system to perturbations that facilitate transitions among stable states. Hence, ecological resilience refers to the width or limit of a stability domain and is defined by the magnitude of disturbance that a system can absorb before it changes stable states (22, 35). The presence of multiple stable states and transitions among them have been described in a range of ecological systems. These include transitions from grass- dominated to woody-dominated semi-arid rangelands in Zimbabwe (60) and Australia (36, 59). In these cases the alternative states are described by domi- nant plant forms, and the disturbance is grazing pressure (59). Other examples include transitions from clear lakes to turbid ones (3, 46) alternative states are indicated by dominant assemblages of primary producers in the water or rooted macrophytes and disturbances include physical variables such as light and tem- perature. Alternative states are also described in populations levels created by interactions among populations (10, 11, 48, 62). Carpenter et al. (3, 5) and Scheffer (46) have used the heuristic of a ball and a cup to highlight differences between these types of resilience. The ball represents the system state and the cup represents the stability domain (Figure 1). An equilibrium exists when the ball sits at the bottom of the cup and disturbances shake the marble to a transient position within the cup. Engineering resilience refers to characteristics of the shape of the cup���the slope of the sides dictate the return time of the ball to the bottom. Ecological resilience suggests that more than one cup exists, and resilience is defined as the width at the top of the cup. Implicit in both of these definitions is the assumption that resilience is a static property of Figure 1 Ball and cup heuristic of system stability. Valleys represent stability domains, balls represent the system, and arrows represent disturbances. Engineering resilience is de- termined by the slopes in the stability landscapes, whereas ecological resilience is described as the width. Adaptive capacity refers to the ability of the system to remain in a stability domain, as the shape of the domain changes (as shown by the three slices or landscapes). Annu. Rev. Ecol. Syst. 2000.31:425-439. Downloaded from arjournals.annualreviews.org by Universidad de Chile on 01/29/08. For personal use only.

P1: FXY September 15, 2000 20:11 Annual Reviews AR113.18 428 GUNDERSON systems. That is, once defined, the shape of the cup remains fixed over time. But recent work indicates that stability domains are dynamic and variable. Adaptive Capacity Many of the manifestations of human-induced state changes in ecosystems result from alteration of the key variables that influence the under- lying stability domains. The key variables that configure these stability domains change at relatively slow rates (without human intervention). Examples include nutrients in wetlands and lakes (5, 46), species compositions in rangelands (56, 59) or trophic relationships (4). Using the ball in cup heuristic, the shape of the cup is subject to change, altering both stability (return time) and resilience (width of stability domain). Scheffer et al. (46) depict this as multiple stability landscapes (three slices in Figure 1). The property of an ecosystem that describes this change in stability landscapes and resilience is referred to as adaptive capacity (19). Ecosystem Dynamics and Multiple Stable States The previous section outlined a contrast among three views of resilience. All describe aspects of change in ecosystems and the degree of that change. But much of the literature over the last 30 years has addressed whether multiple stable states exist in ecosystems, and if so what mediates transition among them. There is a growing body of literature that documents transitions among stability domains in a variety of ecosystems (4, 21, 35, 38, 59, 60). Many of those systems are influenced by human activities, which has led to a confounding problem around ecological resilience. Some authors (49) suggest that alternative stable states do not exist in systems untouched by humans, while others (10, 47) indicate that these are and have been part of the dynamics of systems with or without humans. Without treading on the question of whether people are or are not natural parts of ecosystems, three examples are presented suggesting that people do change the resilience of system. One involves lake systems, another wetlands, and the other semi-arid rangeland. In each example, the alternative states are discussed, as are the mechanisms that result in the transitions and those processes that contribute or detract from ecological resilience. Shallow Lakes Limnologists have long recognized the existence of qualitative differences in the state of lakes. In shallow lakes, two alternative states can be characterized as (a) clear water and rooted macrophytes or (b) turbid water with planktonic algae (45, 46). Each of these states is relatively stable due to interactions among nutrients, the types of vegetation, and light penetration (Figure 1). In the clear water state, sediments, and nutrient cycling are stabilized by rooted vegetation (45, 46). The turbid state persists when wind-driven mixing resuspends sediments. The sediments and phytoplankton in the water column decrease light penetration, thereby curtailing establishment of benthic vegetation (45, 46). Transitions between these two states can be mediated by trophic relationships. Decreasing stocks of planktivorous fish can create a shift from a turbid to a clear Annu. Rev. Ecol. Syst. 2000.31:425-439. Downloaded from arjournals.annualreviews.org by Universidad de Chile on 01/29/08. For personal use only.

P1: FXY September 15, 2000 20:11 Annual Reviews AR113.18 RESILIENCE-THEORY AND PRACTICE 429 lake. As predation on herbivorous zooplankton decreases, their populations in- crease, leading to an increase in herbivory and a reduction in phytoplankton biomass. Increased light penetration and available nutrients then lead to estab- lishment of rooted vegetation (45). In the other direction, shifts from the clear to turbid state can result from overgrazing of benthic vegetation by fish or waterfowl (45). The shift between stable states is hysteretic���the disturbances that influence change in one direction do not have similar impacts in the opposite direction (45). Wetlands Nutrient enrichment in the freshwater marshes of the Everglades caused the loss of resilience. The Everglades is an oligotrophic wetland, limited primar- ily by phosphorus (50). For the past 5000 years or so, the ecosystem effectively self-organized around this low nutrient status, pulsed by annual wet/dry cycles and by decadal recycling associated with fires (17). The resulting landscape mosaic was comprised of sawgrass marshes and wet prairies interspersed with small tree islands (7, 33, 50). In the late 1970s and early 1980s, large-scale vegetation changes were noticed in the regions downstream from the Everglades agricultural area. Sawgrass marshes and wet prairies had become dominated by a single species���cattail (8). The con- version was attributed to a slow increase in the concentration of soil phosphorus, and a disturbance, such as fire, drought or freeze. Key ecosystem processes and structures occur at various spatial and temporal scales. The vegetation structures represent the most rapidly changing variables, with plant turnover times on the order of 5 to 10 years (8). Fires operate on re- turn frequencies of 10 to 20 y (20, 53). Other disturbances such as freezes and droughts occur on multiple decade return times (20, 53). The soil phosphorus concentrations are the slowest of the variables, with turnover times on the order of centuries (8). The resilience of the freshwater marshes is related to the soil nutrient content. The alternative stability domains are characterized by the dominant plant species sawgrass or wet prairie communities dominate on sites with low nutrients, and cattail dominates on sites with higher soil phosphorus concentrations. Following a disturbance, it is the soil phosphorus level that determines which of these species dominate. Semi-arid Rangelands Savanna rangelands are found in climatic regimes of hot, rainy summers and mild, dry winters. These systems have high productivity and support a diverse assemblage of perennial and annual grasses and few woody plants. Key biophysical processes in these systems include variation in rainfall, fires, and grazing. Walker (59) and Ludwig et al. (36) identify alternative stable states as either woody/grass coverage, or woody thicket. The transition between these states is mediated by grazing pressures that remove either drought-tolerant or perennial grasses (36, 59). If grazing pressures are high, the perennial grass abundance is decreased, leading to an increased abundance of woody plants. Once Annu. Rev. Ecol. Syst. 2000.31:425-439. Downloaded from arjournals.annualreviews.org by Universidad de Chile on 01/29/08. For personal use only.