Gradual regime shifts in spatially extended ecosystems

Ecosystem regime shifts are regarded as abrupt global transitions from one stable state to an alternative stable state, induced by slow environmental changes or by global disturbances. Spatially extended ecosystems, however, can also respond to local disturbances by the formation of small domains of the alternative state. Such a response can lead to gradual regime shifts involving front propagation and the coalescence of alternative-state domains. When one of the states is spatially patterned, a multitude of intermediate stable states appears, giving rise to step-like gradual shifts with extended pauses at these states. Using a minimal model, we study gradual state transitions and show that they precede abrupt transitions. We propose indicators to probe gradual regime shifts, and suggest that a combination of abrupt-shift indicators and gradual-shift indicators might be needed to unambiguously identify regime shifts. Our results are particularly relevant to desertification in drylands where transitions to bare soil take place from spotted vegetation, and the degradation process appears to involve step-like events of local vegetation mortality caused by repeated droughts.     

Synergistic effects of drought and deforestation on the resilience of the south-eastern Amazon rainforest

The south-eastern Amazon rainforest is subject to ongoing deforestation and is expected to become drier due to climate change. Recent analyses of the distribution of tree cover in the tropics show three modes that have been interpreted as representing alternative stable states: forest, savanna and treeless states. This situation implies that a change in environmental conditions, such as in the climate, could cause critical transitions from a forest towards a savanna ecosystem. Shifts to savanna might also occur if perturbations such as deforestation exceed a critical threshold. Recovering the forest would be difficult as the savanna will be stabilized by a feedback between tree cover and fire. Here we explore how environmental changes and perturbations affect the forest by using a simple model with alternative tree-cover states. We focus on the synergistic effects of precipitation reduction and deforestation on the probability of regime shifts in the south-eastern Amazon rainforest. The analysis indicated that in a large part of the south-eastern Amazon basin rainforest and savanna could be two alternative states, although massive forest dieback caused by mean-precipitation reduction alone is unlikely. However, combinations of deforestation and climate change triggered up to 6.6 times as many local regime shifts than the two did separately, causing large permanent forest losses in the studied region. The results emphasize the importance of reducing deforestation rates in order to prevent a climate-induced dieback of the south-eastern Amazon rainforest.     

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.     

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.     

Alternative (un)stable states in a stochastic predator–prey model

Stochastic models sometimes behave qualitatively differently from their deterministic analogues. We explore the implications of this in ecosystems that shift suddenly from one state to another. This phenomenon is usually studied through deterministic models with multiple stable equilibria under a single set of conditions, with stability defined through linear stability analysis. However, in stochastic systems, some unstable states can trap stochastic dynamics for long intervals, essentially masquerading as additional stable states. Using a predator–prey model, we demonstrate that this effect is sufficient to make a stochastic system with one stable state exhibit the same characteristics as an analogous system with alternative stable states. Although this result is surprising with respect to how stability is defined by standard analyses, we show that it is well-anticipated by an alternative approach based on the system's “quasi-potential.” Broadly, understanding the risk of sudden state shifts will require a more holistic understanding of stability in stochastic systems.     

生态系统状态跃变的早期预警信号及检测

生态系统在气候变化和土地利用及人类活动等的影响下其状态会由某一稳态转变到另一稳态。由于环境压力的复杂性、非线性、随机性等特征，往往导致状态转变表现为非线性、突变、跃变等特点。准确界定系统状态跃变的拐点或阈值点存在很大的挑战，而捕捉接近临界拐点前的生态系统结构和属性上的变化特征作为早期预警信号是切实可行的。早期预警信号理论经历理论框架构建、方法确立、机理认知等近半个多世纪的探索，已经由最初的通过仅依赖检测临界点恢复力的速率减慢、方差增加、系统自相关增强等统计学信号过度到更加多样化的检测方法，如检测系统组分属性的变化特征，诊断系统组分各属性之间的关系变化，系统组分的性状变化、系统组分网络结构变化等等，并且试图整合多信号提高预警的精确性。利用来自自然生态系统的长时间高密度数据集和空间代替时间的数据集，基于多度及性状信号的早期预警，结合稳定性、临界恢复力的减速、以及统计参数的指示作用对系统跃变进行早期诊断和预警是预测生态学的主旨。早期预警信号的深入研究不仅能够完善已有理论的不足，同时还能够为生态系统的保护和管理提供切实有效的理论指导。     

Crossing habitat boundaries: coupling dynamics of ecosystems through complex life cycles

Ecosystems are often indirectly connected through consumers with complex life cycles (CLC), in which different life stages inhabit different ecosystems. Using a structured consumer resource model that accounts for the independent effects of two resources on consumer growth and reproductive rates, we show that such indirect connections between ecosystems can result in alternative stable states characterized by adult-dominated and juvenile-dominated consumer populations. As a consequence, gradual changes in ecosystem productivity or mortality rates of the consumer can lead to dramatic and abrupt regime shifts across different ecosystems, hysteresis and counterintuitive changes in the consumer abundances. Whether these counter intuitive or abrupt responses occur depend on the relative productivity of both habitats and which consumer life-stage inhabits the manipulated ecosystem. These results demonstrate the strong yet complex interactions between ecosystems coupled through consumers with CLC and the need to think across ecosystems to reliably predict the consequences of natural or anthropogenic changes.     

Regime shifts in exploited marine food webs: detecting mechanisms underlying alternative stable states using size-structured community dynamics theory

Many marine ecosystems have undergone ‘regime shifts’, i.e. abrupt reorganizations across trophic levels. Establishing whether these constitute shifts between alternative stable states is of key importance for the prospects of ecosystem recovery and for management. We show how mechanisms underlying alternative stable states caused by predator–prey interactions can be revealed in field data, using analyses guided by theory on size-structured community dynamics. This is done by combining data on individual performance (such as growth and fecundity) with information on population size and prey availability. We use Atlantic cod (Gadus morhua) and their prey in the Baltic Sea as an example to discuss and distinguish two types of mechanisms, ‘cultivation-depensation’ and ‘overcompensation’, that can cause alternative stable states preventing the recovery of overexploited piscivorous fish populations. Importantly, the type of mechanism can be inferred already from changes in the predators'' body growth in different life stages. Our approach can thus be readily applied to monitored stocks of piscivorous fish species, for which this information often can be assembled. Using this tool can help resolve the causes of catastrophic collapses in marine predatory–prey systems and guide fisheries managers on how to successfully restore collapsed piscivorous fish stocks.     

Do herbivores cause habitat degradation or vegetation state transition? Evidence from the tundra

Range expansion and increasing densities of large herbivores are held responsible for large-scale habitat degradation in a wide range of natural and semi-natural ecosystems. Herbivore-driven ecosystem changes frequently represent predictable transitions from one vegetation state to another. Whether such predictable changes justify the value judgement 'habitat degradation' may be debatable as this strongly depends on individual perspective.
To further the debate on herbivore-driven habitat degradation, I apply the concept of alternative stable states to arctic tundra as a framework to capture predictable stepwise vegetation transitions in which the productivity and hence herbivore-carrying capacity increases with grazing pressure. Specifically, evidence is provided that large parts of the tundra biome can be in either of three relatively discrete vegetation states and that changes in reindeer/caribou density are responsible for sudden, predictable but often reversible state transitions. From this, it appears that the relatively rapidly emerging vegetation changes do not necessarily equate to habitat degradation, but in many cases reflect predictable vegetation change. Acknowledgement of the existence of predictable state transitions in tundra ecosystems may help to evaluate the observed radical vegetation changes occurring throughout the reindeer/caribou range.     

Early detection of ecosystem regime shifts: a multiple method evaluation for management application

Critical transitions between alternative stable states have been shown to occur across an array of complex systems. While our ability to identify abrupt regime shifts in natural ecosystems has improved, detection of potential early-warning signals previous to such shifts is still very limited. Using real monitoring data of a key ecosystem component, we here apply multiple early-warning indicators in order to assess their ability to forewarn a major ecosystem regime shift in the Central Baltic Sea. We show that some indicators and methods can result in clear early-warning signals, while other methods may have limited utility in ecosystem-based management as they show no or weak potential for early-warning. We therefore propose a multiple method approach for early detection of ecosystem regime shifts in monitoring data that may be useful in informing timely management actions in the face of ecosystem change.     

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。     

Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea

Marine ecosystems such as the Baltic Sea are currently under strong atmospheric and anthropogenic pressure. Besides natural and human-induced changes in climate, major anthropogenic drivers such as overfishing and anthropogenic eutrophication are significantly affecting ecosystem structure and function. Recently, studies demonstrated the existence of alternative stable states in various terrestrial and aquatic ecosystems. These so-called ecosystem regime shifts have been explained mainly as a result of multiple causes, e.g. climatic regime shifts, overexploitation or a combination of both. The occurrence of ecosystem regime shifts has important management implications, as they can cause significant losses of ecological and economic resources. Because of hysteresis in ecosystem responses, restoring regimes considered as favourable may require drastic and expensive management actions. Also the Baltic Sea, the largest brackish water body in the world ocean, and its ecosystems are strongly affected by atmospheric and anthropogenic drivers. Here, we present results of an analysis of the state and development of the Central Baltic Sea ecosystem integrating hydroclimatic, nutrient, phyto- and zooplankton as well as fisheries data. Our analyses of 52 biotic and abiotic variables using multivariate statistics demonstrated a major reorganization of the ecosystem and identified two stable states between 1974 and 2005, separated by a transition period in 1988–1993. We show the change in Baltic ecosystem structure to have the characteristics of a discontinuous regime shift, initiated by climate-induced changes in the abiotic environment and stabilized by fisheries-induced feedback loops in the food web. Our results indicate the importance of maintaining the resilience of an ecosystem to atmospherically induced environmental change by reducing the anthropogenic impact.     

Changing skewness: an early warning signal of regime shifts in ecosystems

Empirical evidence for large-scale abrupt changes in ecosystems such as lakes and vegetation of semi-arid regions is growing. Such changes, called regime shifts, can lead to degradation of ecological services. We study simple ecological models that show a catastrophic transition as a control parameter is varied and propose a novel early warning signal that exploits two ubiquitous features of ecological systems: nonlinearity and large external fluctuations. Either reduced resilience or increased external fluctuations can tip ecosystems to an alternative stable state. It is shown that changes in asymmetry in the distribution of time series data, quantified by changing skewness, is a model-independent and reliable early warning signal for both routes to regime shifts. Furthermore, using model simulations that mimic field measurements and a simple analysis of real data from abrupt climate change in the Sahara, we study the feasibility of skewness calculations using data available from routine monitoring.     

Marine protected areas in 'nonlinear' ecosystems

The very large changes observed within marine communities, owing to excessive harvesting, have been attributed to switches between alternative stable states. Correspondingly large reductions in overall fishing effort are usually difficult to implement. For such 'nonlinear' ecosystems, introducing large marine protected areas, with low to zero harvesting, but without reduction in overall fishing effort, can give a marked increase in total yield of the depleted stocks. These increases, however, are still less than can be achieved by reducing fishing effort.     

Slow recovery from perturbations as a generic indicator of a nearby catastrophic shift

The size of the basin of attraction in ecosystems with alternative stable states is often referred to as "ecological resilience." Ecosystems with a low ecological resilience may easily be tipped into an alternative basin of attraction by a stochastic event. Unfortunately, it is very difficult to measure ecological resilience in practice. Here we show that the rate of recovery from small perturbations (sometimes called "engineering resilience") is a remarkably good indicator of ecological resilience. Such recovery rates decrease as a catastrophic regime shift is approached, a phenomenon known in physics as "critical slowing down." We demonstrate the robust occurrence of critical slowing down in six ecological models and outline a possible experimental approach to quantify differences in recovery rates. In all the models we analyzed, critical slowing down becomes apparent quite far from a threshold point, suggesting that it may indeed be of practical use as an early warning signal. Despite the fact that critical slowing down could also indicate other critical transitions, such as a stable system becoming oscillatory, the robustness of the phenomenon makes it a promising indicator of loss of resilience and the risk of upcoming regime shifts in a system.     

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.     

Low biodiversity state persists two decades after cessation of nutrient enrichment

Although nutrient enrichment frequently decreases biodiversity, it remains unclear whether such biodiversity losses are readily reversible, or are critical transitions between alternative low‐ and high‐diversity stable states that could be difficult to reverse. Our 30‐year grassland experiment shows that plant diversity decreased well below control levels after 10 years of chronic high rates (95–270 kg N ha⁻¹ year⁻¹) of nitrogen addition, and did not recover to control levels 20 years after nitrogen addition ceased. Furthermore, we found a hysteretic response of plant diversity to increases and subsequent decreases in soil nitrate concentrations. Our results suggest that chronic nutrient enrichment created an alternative low‐diversity state that persisted despite decreases in soil nitrate after cessation of nitrogen addition, and despite supply of propagules from nearby high‐diversity plots. Thus, the regime shifts between alternative stable states that have been reported for some nutrient‐enriched aquatic ecosystems may also occur in grasslands.     

Early warning signals of demographic regime shifts in invading populations

The Allee effect can cause alternative stable states in population abundance of invasive species. Sudden eruption of invading populations from low to high abundance may be viewed as a regime shift from one alternative state to another. Previous research proposed several types of early warning signals to predict regime shifts in ecological systems such as polluted lakes and semiarid grasslands. This paper explores theoretically the potential of such indicators in predicting demographic regime shifts of invading populations. I analyzed a stochastic differential equation model for the population dynamics of an invasive species subject to Allee effects and propagule pressure. Diffusion approximation to the stochastic model suggests that persistent propagule pressure makes demographic regime shifts inevitable, but Allee effects can lengthen the mean time until regime shifts virtually indefinitely. To compare the potential of indicators, I examined standard deviation, skewness, and estimated return rates of longitudinal population abundance. I found that standard deviation showed a distinct increase as regime shifts became more likely, but skewness and return rates showed no clear trends. This result suggests that standard deviation might be a useful warning signal for forecasting an impending demographic regime shift of invading populations during the period when their abundance is still low.     

Large species shifts triggered by small forces

Changes in species composition of communities seem to proceed gradually at first sight, but remarkably rapid shifts are known to occur. Although disrupting disturbances seem an obvious explanation for such shifts, evidence for large disturbances is not always apparent. Here we show that complex communities tend to move through occasional catastrophic shifts in response to gradual environmental change or evolution. This tendency is caused by multiple attractors that may exist in such systems. We show that alternative attractors arise robustly in randomly generated multispecies models, especially if competition is symmetrical and if interspecific competition is allowed to exceed intraspecific competition. Inclusion of predators as a second trophic level did not alter the results greatly, although it reduced the probability of alternative attractors somewhat. These results suggest that alternative attractors may commonly arise from interactions between large numbers of species. Consequently, the response of complex communities to environmental change is expected to be characterized by hysteresis and sudden shifts. Some unexplained regime shifts observed in ecosystems could be related to alternative attractors arising from complex species interactions. Additionally, our results support the idea that ancient mass extinctions may partly be due to an intrinsic loss of stability of species configurations.     

Alternative Stable States Driven by Density-Dependent Toxicity

Many populations are exposed to naturally occurring or synthetic toxicants. An increasing number of studies demonstrate that the toxicity of such compounds is not only dependent on the concentration or load, but also on the biomass or density of exposed organisms. At high biomass, organisms may be able to alleviate adverse effects of the toxicant by actively lowering ambient concentrations through either a joint detoxification mechanism or growth dilution. We show in a conceptual model that this mechanism may potentially lead to alternative stable states if the toxicant is lethal at low densities of organisms, whereas a high density is able to reduce the toxicant concentrations to sub-lethal levels. We show in an example that this effect may be relevant in real ecosystems. In an earlier published experimental laboratory study, we demonstrated that ammonia toxicity in eelgrass is highly dependent on the eelgrass shoot density. Here, we used the results of these experiments to construct a model describing the complex interactions between the temperate seagrass Zostera marina and potentially lethal ammonia. Analyses of the model show that alternative stable states are indeed present over wide ranges of key-parameter settings, suggesting that the mechanism might be important especially in sheltered, eutrophicated estuaries where mixing of the water layer is poor. We argue that the same mechanism could cause alternative stable states in other biological systems as well.