When are alternative stable states more likely to occur?

T. Fukami and W. G. Lee argue that the logical expectation from ecological theory is that competitively-structured assemblages will be more likely to exhibit alternative stable states than abiotically-structured assemblages. We suggest that there are several important misinterpretations in their arguments, and that the substance of their hypothesis has both a weak basis in ecological theory and is not supported by empirical evidence which shows that alternative stable states occur more frequently in natural systems subject to moderate- to harsh abiotic extremes. While this debate is founded in ecological theory, it has important applied implications for restoration management. Sound theoretical predictions about when to expect alternative stable states can only aid more effective restoration if theoretical expectations can be shown to translate into predictable empirical outcomes. If strongly abiotically- or disturbance-structured systems are more likely to exhibit catastrophic phase shifts in community structure that can be resilient to management efforts, then restoration ecologists will need to treat these systems differently in terms of the types of management inputs that are required.     

生态系统的多稳态与突变

许多生态系统可能在短时间内发生难以预料的状态突变, 其中一些生态系统突变的机理可以用多稳态理论进行解释。近年来生态系统的多稳态和突变现象及其机理吸引了研究者和管理者的广泛关注。本文重点对生态系统多稳态的理论基础、识别方法及稳态转换发生的早期预警信号进行综述, 并基于典型生态系统过程对现实世界中可能观测到的稳态转换进行实例分析, 最后对多稳态概念框架和理论应用中的潜在争议进行讨论, 以期为非线性生态系统动态的理论研究、管理实践和生物多样性保护等提供参考。     

Are systems with strong underlying abiotic regimes more likely to exhibit alternative stable states?

Suding et al. (2004) demonstrate how conceptual advances in alternative ecosystem states theory have led to a greater understanding of why degraded systems are often resilient to restoration management. In their review they pose one (of several) ‘outstanding’ questions (Box 3 in Suding et al. 2004 ): “Are there predictable characteristics that indicate when a system will follow a successional pathway and/or that indicate the presence or absence of alternative ecosystem states?” We suggest that the persistence of alternative stable states might be predicted from simple consideration of assembly rules for systems structured along a gradient of environmental adversity. We raise the hypothesis that strongly abiotically‐ or disturbance‐structured assemblages, with nonrandom trait under‐dispersion ( Weiher and Keddy 1995 ), are more likely to exhibit catastrophic phase shifts in community structure than assemblages which are weakly structured by environmental adversity.     

社会-生态系统恢复力的测量方法综述

恢复力和社会-生态系统研究的理论及实践近年来在西方较为流行,然而经过几十年发展,学术界仍旧没有对恢复力的概念达成一致,相应的测量方法更是多种多样。基于恢复力理论对系统相对稳定状态和边界的假设以及恢复力概念3个阶段的演变和理论的发展,总结了测量恢复力的5种方法,得出恢复力测量的3个发展现状或趋势:阈值和断裂点方法依旧是量化恢复力的基本方法;恢复力测量从关注时间转向空间,关注生态转向社会和社会-生态;复杂学和多学科融合的方法是未来发展的主要方向。     

Alternative stable states in inherently unstable systems

Alternative stable states are nontransitory states within which communities can exist. However, even highly dynamic communities can be viewed within the framework of stable‐state theory if an appropriate “ecologically relevant” time scale is identified. The ecologically relevant time scale for dynamic systems needs to conform to the amount of time needed for a system's community to complete an entire cycle through its normal range of variation. For some systems, the ecologically relevant period can be relatively short (eg, tidal systems), for others it can be decadal (eg, prairie wetlands). We explore the concept of alternative stable states in unstable systems using the highly dynamic wetland ecosystems of North America's Prairie Pothole Region. The communities in these wetland ecosystems transition through multiple states in response to decadal‐long climate oscillations that cyclically influence ponded‐water depth, permanence, and chemistry. The perspective gained by considering dynamic systems in the context of stable‐state theory allows for an increased understanding of how these systems respond to changing drivers that can push them past tipping points into alternative states. Incorporation of concepts inherent to stable‐state theory has been suggested as a key scientific element upon which to base sustainable environmental management.     

Multiplicity of stable states in freshwater systems

It is shown with the use of minimal models that several ecological relationships in freshwater systems potentially give rise to the existence of alternative equilibria over a certain range of nutrient values. The existence of alternative stable states has some implications for the management of such systems. An important consequence is that signs of eutrophication are only apparent after the occurrence of changes that are very difficult to reverse. Reduction of the nutrient level as a measure to restore such systems gives poor results, but biomanipulation as an additional measure can have significant effects, provided that the nutrient level has been reduced enough to allow the existence of a stable alternative clear water equilibrium.     

A simple histone code opens many paths to epigenetics

Nucleosomes can be covalently modified by addition of various chemical groups on several of their exposed histone amino acids. These modifications are added and removed by enzymes (writers) and can be recognized by nucleosome-binding proteins (readers). Linking a reader domain and a writer domain that recognize and create the same modification state should allow nucleosomes in a particular modification state to recruit enzymes that create that modification state on nearby nucleosomes. This positive feedback has the potential to provide the alternative stable and heritable states required for epigenetic memory. However, analysis of simple histone codes involving interconversions between only two or three types of modified nucleosomes has revealed only a few circuit designs that allow heritable bistability. Here we show by computer simulations that a histone code involving alternative modifications at two histone positions, producing four modification states, combined with reader-writer proteins able to distinguish these states, allows for hundreds of different circuits capable of heritable bistability. These expanded possibilities result from multiple ways of generating two-step cooperativity in the positive feedback - through alternative pathways and an additional, novel cooperativity motif. Our analysis reveals other properties of such epigenetic circuits. They are most robust when the dominant nucleosome types are different at both modification positions and are not the type inserted after DNA replication. The dominant nucleosome types often recruit enzymes that create their own type or destroy the opposing type, but never catalyze their own destruction. The circuits appear to be evolutionary accessible; most circuits can be changed stepwise into almost any other circuit without losing heritable bistability. Thus, our analysis indicates that systems that utilize an expanded histone code have huge potential for generating stable and heritable nucleosome modification states and identifies the critical features of such systems.     

Change in a lake benthic community over a century: evidence for alternative community states

Aquatic communities are one of the most studied systems where alternative states or regime shifts have been detected. We used data spanning a century of time to test whether the zoobenthic community of Lake Mendota, Wisconsin, USA, was relatively stable through time, variable, or whether there was any evidence of alternative community states. We used multivariate statistical analyses to test for community structure similarity and whether detected differences corresponded to major changes in the local environment. Surprisingly, the benthic community in Lake Mendota was not statistically different from the mid 1960s to the present. Similarly, the benthic community was not significantly different from 1914 to the 1950s. However, between the 1950s and mid 1960s there was a dramatic change in the zoobenthic community, including the loss of key taxa and a decrease in the diversity of several major taxa. This dramatic change cannot be attributed to any single environmental factor, and is correlated with multiple factors acting simultaneously, including increased urban development, human population density, intensive agriculture, and the introduction of a major invasive species, Eurasian watermilfoil. The long-term similarity in the benthic community before and after the shift suggests two alternative states that switched with the confluence of multiple stressors.     

Tracking unstable states: ecosystem dynamics in a changing world

Ecological systems can show complex and sometimes abrupt responses to environmental change, with important implications for their resilience. Theories of alternate stable states have been used to predict regime shifts of ecosystems as equilibrium responses to sufficiently slow environmental change. The actual rate of environmental change is a key factor affecting the response, yet we are still lacking a non-equilibrium theory that explicitly considers the influence of this rate of environmental change. We present a metacommunity model of predator–prey interactions displaying multiple stable states, and we impose an explicit rate of environmental change in habitat quality (carrying capacity) and connectivity (dispersal rate). We study how regime shifts depend on the rate of environmental change and compare the outcome with a stability analysis in the corresponding constant environment. Our results reveal that in a changing environment, the community can track states that are unstable in the constant environment. This tracking can lead to regime shifts, including local extinctions, that are not predicted by alternative stable state theory. In our metacommunity, tracking unstable states also controls the maintenance of spatial heterogeneity and spatial synchrony. Tracking unstable states can also lead to regime shifts that may be reversible or irreversible. Our study extends current regime shift theories to integrate rate-dependent responses to environmental change. It reveals the key role of unstable states for predicting transient dynamics and long-term resilience of ecological systems to climate change.     

Abrupt shifts in African savanna tree cover along a climatic gradient

Aim To describe patterns of tree cover in savannas over a climatic gradient and a range of spatial scales and test if there are identifiable climate‐related mean structures, if tree cover always increases with water availability and if there is a continuous trend or a stepwise trend in tree cover. Location Central Tropical Africa. Methods We compared a new analysis of satellite tree cover data with botanical, phytogeographical and environmental data. Results Along the climatic transect, six vegetation structures were distinguished according to their average tree cover, which can co‐occur as mosaics. The resulting abrupt shifts in tree cover were not correlated to any shifts in either environmental variables or in tree species distributions. Main conclusions A strong contrast appears between fine‐scale variability in tree cover and coarse‐scale structural states that are stable over several degrees of latitude. While climate parameters and species pools display a continuous evolution along the climatic gradient, these stable structural states have discontinuous transitions, resulting in regions containing mosaics of alternative stable states. Soils appear to have little effect inside the climatic stable state domains but a strong action on the location of the transitions. This indicates that savannas are patch dynamics systems, prone to feedbacks stabilizing their coarse‐scale structure over wide ranges of environmental conditions.     

Direct experimental evidence for alternative stable states: a review

A large number of studies have presented empirical arguments for the existence of alternative stable states (ASS) in a wide range of ecological systems. However, most of these studies have used non-manipulative, indirect methods, which findings remain open for alternative explanations. Here, we review the direct evidence for ASS resulting from manipulation experiments. We distinguish four conclusive experimental approaches which test for predictions made by the hysteresis effect: (1) discontinuity in the response to an environmental driving parameter, (2) lack of recovery potential after a perturbation, (3) divergence due to different initial conditions and (4) random divergence. Based on an extensive literature search we found 35 corresponding experiments. We assessed the ecological stability of the reported contrasting states using the minimum turnover of individuals in terms of life span and classified the studies according to 4 categories: (1) experimental system, (2) habitat type, (3) involved organisms and (4) theoretical framework. 13 experiments have directly demonstrated the existence of alternative stable states while 8 showed the absence of ASS in other cases. 14 experiments did not fulfil the requirements of a conclusive test, mostly because they applied a too short time scale. We found a bias towards laboratory experiments compared to field experiments in demonstrating bistability. There was no clear pattern of the distribution of ASS over categories. The absence of ASS in 38% of the tested systems indicates that ASS are just one possibility of how ecological systems can behave. The relevance of the concept of ASS for natural systems is discussed, in particular under consideration of the observed laboratory bias, perturbation frequency and variable environments. It is argued, that even for a permanently transient system, alternative attractors may still be of relevance.     

Absolute stability and transitions in ecosystems with a multiplicity of stable states and dispersal

The principle that for a large class of spatially extended dynamic systems with several locally stable states there exists at most one absolutely stable state is applied to population dynamical models with diffusive spatial dispersal. The basic concepts and methods to characterize absolute stability and its limits are presented. Some interesting results concerning the significance of dispersal ability in competing and mutualistic systems are found. The concepts appear of practical importance since only absolutely stable states are resilient against all localized fluctuations and disturbances.     

On Circuit Functionality in Boolean Networks

It has been proved, for several classes of continuous and discrete dynamical systems, that the presence of a positive (resp. negative) circuit in the interaction graph of a system is a necessary condition for the presence of multiple stable states (resp. a cyclic attractor). A positive (resp. negative) circuit is said to be functional when it “generates” several stable states (resp. a cyclic attractor). However, there are no definite mathematical frameworks translating the underlying meaning of “generates.” Focusing on Boolean networks, we recall and propose some definitions concerning the notion of functionality along with associated mathematical results.     

Catastrophic regime shifts in ecosystems: linking theory to observation

Occasionally, surprisingly large shifts occur in ecosystems. Theory suggests that such shifts can be attributed to alternative stable states. Verifying this diagnosis is important because it implies a radically different view on management options, and on the potential effects of global change on such ecosystems. For instance, it implies that gradual changes in temperature or other factors might have little effect until a threshold is reached at which a large shift occurs that might be difficult to reverse. Strategies to assess whether alternative stable states are present are now converging in fields as disparate as desertification, limnology, oceanography and climatology. Here, we review emerging ways to link theory to observation, and conclude that although, field observations can provide hints of alternative stable states, experiments and models are essential for a good diagnosis.     

Marine fisheries as ecological experiments

There are many examples of ecological theory informing fishery management. Yet fisheries also provide tremendous opportunities to test ecological theory through large-scale, repeated, and well-documented perturbations of natural systems. Although treating fisheries as experiments presents several challenges, few comparable tests exist at the ecosystem scale. Experimental manipulations of fish populations in lakes have been widely used to develop and test ecological theory. Controlled manipulation of fish populations in open marine systems is rarely possible, but fisheries data provide a valuable substitute for such manipulations. To highlight the value of marine fisheries data, we review leading ecological theories that have been empirically tested using such data. For example, density dependence has been examined through meta-analysis of spawning stock and recruitment data to show that compensation (higher population growth) occurs commonly when populations are reduced to low levels, while depensation (the Allee effect) is rare. As populations decline, spatial changes typically involve populations contracting into high-density core habitats while abandoning less productive habitats. Fishing down predators may result in trophic cascades, possibly shifting entire ecosystems into alternate stable states, although alternate states can be maintained by both ecological processes and continued fishing pressure. Conversely, depleting low trophic level groups may affect central-place foragers, although these bottom–up effects rarely appear to impact fish—perhaps because many fish populations have been reduced to the point that they are no longer prey limited. Fisheries provide empirical tests for diversity–stability relations: catch data suggest that more diverse systems recover faster and provide more stable returns than less diverse systems. Fisheries have also provided examples of the tragedy of the commons, as well as counter-examples where common property resources have been managed successfully. We also address two barriers to use of fisheries data to answer ecological questions: differences in terminology for similar concepts and misuse of records of fishery landings (catch data) as a proxy for biomass trends.     

Alternative logical states

N. W. H. Mason, J. B. Wilson and J. B. Steel argue that there is no logical conceptual basis, and no empirical data, to support an association between environmental adversity and the occurrence of alternative stable states. While we agree that robust debate on the relative frequency of occurrence of alternative stable states is valuable, any apparent logic in their argument is confounded by misinterpretation and direct misrepresentation of our earlier arguments ( Didham et al. 2005 ), despite the fact that we clarified many of the same issues in response to T. Fukami and W. G. Lee ( Didham and Norton 2006 ). Opinion, not logic or evidence, underlies Mason, Wilson and Steel's argument, and this does little to further our understanding of why some systems exhibit alternative stable states that are resilient to restoration management efforts.     

Potential for Sudden Shifts in Transient Systems: Distinguishing Between Local and Landscape-Scale Processes

Thorough understanding of the potential for threshold dynamics and catastrophic shifts to occur in natural systems is of great importance for ecosystem conservation and restoration. However, verifying the presence of alternative stable states, one of the theoretical explanations for sudden shifts in natural systems, has proven to be a major challenge. We examine processes on local and landscape scales in salt-marsh pioneer zones, to assess the presence of alternative stable states in this system. To that end, we investigated the presence of typical characteristics of alternative stable states: bimodality and threshold dynamics. We also studied whether vegetation patches remained stable over long time periods. Analysis of false-color aerial photographs revealed clear bimodality in plant biomass distribution. By transplanting Spartina anglica plants of three different biomass classes on three geographically different marshes, we showed that a biomass threshold limits the establishment of Spartina patches, potentially explaining their patchy distribution. The presence of bimodality and biomass thresholds points to the presence of alternative stable states and the potential for sudden shifts, at small, within-patch scales and on short time scales. However, overlay analysis of aerial photographs from a salt marsh in The Netherlands, covering a time span of 22 years, revealed that there was little long-term stability of patches, as vegetation cover in this area is slowly increasing. Our results suggest that the concept of alternative stable states is applicable to the salt-marsh pioneer vegetation on small spatio-temporal scales. However, the concept does not apply to long-term dynamics of decades or centuries of heterogeneous salt-marsh pioneer zones, as landscape-scale processes may determine the large-scale dynamics of salt marshes. Hence, our results provide the interesting perspective that threshold dynamics may occur in systems with, on the long term, only a single stable state. Author Contributions: Bregje van Wesenbeeck executed the major part of this research and wrote this paper. Johan van de Koppel was involved in every part of this study and restructured major parts of this paper. Peter Herman helped with statistical analyses. Mark Bertness adjusted the design of this study and provided new views. Daphne van der Wal performed GIS analyses. Jan Bakker supervised and facilitated field work. Tjeerd Bouma supervised design of study and paper and substantially contributed to the writing of this paper. All authors commented on several drafts of this paper.     

Bistable responses in bacterial genetic networks: designs and dynamical consequences

A key property of living cells is their ability to react to stimuli with specific biochemical responses. These responses can be understood through the dynamics of underlying biochemical and genetic networks. Evolutionary design principles have been well studied in networks that display graded responses, with a continuous relationship between input signal and system output. Alternatively, biochemical networks can exhibit bistable responses so that over a range of signals the network possesses two stable steady states. In this review, we discuss several conceptual examples illustrating network designs that can result in a bistable response of the biochemical network. Next, we examine manifestations of these designs in bacterial master-regulatory genetic circuits. In particular, we discuss mechanisms and dynamic consequences of bistability in three circuits: two-component systems, sigma-factor networks, and a multistep phosphorelay. Analyzing these examples allows us to expand our knowledge of evolutionary design principles networks with bistable responses.     

Spatial correlation as leading indicator of catastrophic shifts

Generic early-warning signals such as increased autocorrelation and variance have been demonstrated in time-series of systems with alternative stable states approaching a critical transition. However, lag times for the detection of such leading indicators are typically long. Here, we show that increased spatial correlation may serve as a more powerful early-warning signal in systems consisting of many coupled units. We first show why from the universal phenomenon of critical slowing down, spatial correlation should be expected to increase in the vicinity of bifurcations. Subsequently, we explore the applicability of this idea in spatially explicit ecosystem models that can have alternative attractors. The analysis reveals that as a control parameter slowly pushes the system towards the threshold, spatial correlation between neighboring cells tends to increase well before the transition. We show that such increase in spatial correlation represents a better early-warning signal than indicators derived from time-series provided that there is sufficient spatial heterogeneity and connectivity in the system.     

Shallow lakes theory revisited: various alternative regimes driven by climate,nutrients, depth and lake size

Shallow lakes have become the archetypical example of ecosystems with alternative stable states. However, since the early conception of that theory, the image of ecosystem stability has been elaborated for shallow lakes far beyond the simple original model. After discussing how spatial heterogeneity and fluctuation of environmental conditions may affect the stability of lakes, we review work demonstrating that the critical nutrient level for lakes to become turbid is higher for smaller lakes, and seems likely to be affected by climatic change too. We then show how the image of just two contrasting states has been elaborated. Different groups of primary producers may dominate shallow lakes, and such states dominated by a particular group may often represent alternative stable states. In tropical lakes, or small stagnant temperate waters, free-floating plants may represent an alternative stable state. Temperate shallow lakes may be dominated alternatively by charophytes, submerged angiosperms, green algae or cyanobacteria. The change of the lake communities along a gradient of eutrophication may therefore be seen as a continuum in which gradual species replacements are interrupted at critical points by more dramatic shifts to a contrasting alternative regime dominated by different species. The originally identified shift between a clear and a turbid state remains one of the more dramatic examples, but is surely not the only discontinuity that can be observed in the response of these ecosystems to environmental change.