Phase-separation physics underlies new theory for the resilience of patchy ecosystems.

Spatial self-organization of ecosystems into large-scale (from micron to meters) patterns is an important phenomenon in ecology, enabling organisms to cope with harsh environmental conditions and buffering ecosystem degradation. Scale-dependent feedbacks provide the predominant conceptual framework for self-organized spatial patterns, explaining regular patterns observed in, e.g., arid ecosystems or mussel beds. Here, we highlight an alternative mechanism for self-organized patterns, based on the aggregation of a biotic or abiotic species, such as herbivores, sediment, or nutrients. Using a generalized mathematical model, we demonstrate that ecosystems with aggregation-driven patterns have fundamentally different dynamics and resilience properties than ecosystems with patterns that formed through scale-dependent feedbacks. Building on the physics theory for phase-separation dynamics, we show that patchy ecosystems with aggregation patterns are more vulnerable than systems with patterns formed through scale-dependent feedbacks, especially at small spatial scales. This is because local disturbances can trigger large-scale redistribution of resources, amplifying local degradation. Finally, we show that insights from physics, by providing mechanistic understanding of the initiation of aggregation patterns and their tendency to coarsen, provide a new indicator framework to signal proximity to ecological tipping points and subsequent ecosystem degradation for this class of patchy ecosystems.

Spatially explicit removal strategies increase the efficiency of invasive plant species control.

Effective management strategies are needed to control expansion of invasive alien plant species and attenuate economic and ecological impacts. While previous theoretical studies have assessed optimal control strategies that balance economic costs and ecological benefits, less attention has been paid to the ways in which the spatial characteristics of individual patches may mediate the effectiveness of management strategies. We developed a spatially explicit cellular automaton model for invasive species spread, and compared the effectiveness of seven control strategies. These control strategies used different criteria to prioritize the removal of invasive species patches from the landscape. The different criteria were related to patch size, patch geometry, and patch position within the landscape. Effectiveness of strategies was assessed for both seed dispersing and clonally expanding plant species. We found that, for seed-dispersing species, removal of small patches and removal of patches that are isolated within the landscape comprised relatively effective control strategies. For clonally expanding species, removal of patches based on their degree of isolation and their geometrical properties comprised relatively effective control strategies. Subsequently, we parameterized the model to mimic the observed spatial distribution of the invasive species Antigonon leptopus on St. Eustatius (northern Caribbean). This species expands clonally and also disperses via seeds, and model simulations showed that removal strategies focusing on smaller patches that are more isolated in the landscape would be most effective and could increase the effectiveness of a 10-yr control strategy by 30-90%, as compared to random removal of patches. Our study emphasizes the potential for invasive plant species management to utilize recent advances in remote sensing, which enable mapping of invasive species at the high spatial resolution needed to quantify patch geometries. The presented results highlight how this spatial information can be used in the design of more effective invasive species control strategies.

Multistability of model and real dryland ecosystems through spatial self-organization.

Spatial self-organization of dryland vegetation constitutes one of the most promising indicators for an ecosystem's proximity to desertification. This insight is based on studies of reaction-diffusion models that reproduce visual characteristics of vegetation patterns observed on aerial photographs. However, until now, the development of reliable early warning systems has been hampered by the lack of more in-depth comparisons between model predictions and real ecosystem patterns. In this paper, we combined topographical data, (remotely sensed) optical data, and in situ biomass measurements from two sites in Somalia to generate a multilevel description of dryland vegetation patterns. We performed an in-depth comparison between these observed vegetation pattern characteristics and predictions made by the extended-Klausmeier model for dryland vegetation patterning. Consistent with model predictions, we found that for a given topography, there is multistability of ecosystem states with different pattern wavenumbers. Furthermore, observations corroborated model predictions regarding the relationships between pattern wavenumber, total biomass, and maximum biomass. In contrast, model predictions regarding the role of slope angles were not corroborated by the empirical data, suggesting that inclusion of small-scale topographical heterogeneity is a promising avenue for future model development. Our findings suggest that patterned dryland ecosystems may be more resilient to environmental change than previously anticipated, but this enhanced resilience crucially depends on the adaptive capacity of vegetation patterns.

The effect of climate change on the resilience of ecosystems with adaptive spatial pattern formation.

In a rapidly changing world, quantifying ecosystem resilience is an important challenge. Historically, resilience has been defined via models that do not take spatial effects into account. These systems can only adapt via uniform adjustments. In reality, however, the response is not necessarily uniform, and can lead to the formation of (self-organised) spatial patterns - typically localised vegetation patches. Classical measures of resilience cannot capture the emerging dynamics in spatially self-organised systems, including transitions between patterned states that have limited impact on ecosystem structure and productivity. We present a framework of interlinked phase portraits that appropriately quantifies the resilience of patterned states, which depends on the number of patches, the distances between them and environmental conditions. We show how classical resilience concepts fail to distinguish between small and large pattern transitions, and find that the variance in interpatch distances provides a suitable indicator for the type of imminent transition. Subsequently, we describe the dependency of ecosystem degradation based on the rate of climatic change: slow change leads to sporadic, large transitions, whereas fast change causes a rapid sequence of smaller transitions. Finally, we discuss how pre-emptive removal of patches can minimise productivity losses during pattern transitions, constituting a viable conservation strategy.

Increased aridity drives post-fire recovery of Mediterranean forests towards open shrublands.

Recent observations suggest that repeated fires could drive Mediterranean forests to shrublands, hosting flammable vegetation that regrows quickly after fire. This feedback supposedly favours shrubland persistence and may be strengthened in the future by predicted increased aridity. An assessment was made of how fires and aridity in combination modulated the dynamics of Mediterranean ecosystems and whether the feedback could be strong enough to maintain shrubland as an alternative stable state to forest. A model was developed for vegetation dynamics, including stochastic fires and different plant fire-responses. Parameters were calibrated using observational data from a period up to 100 yr ago, from 77 sites with and without fires in Southeast Spain and Southern France. The forest state was resilient to the separate impact of fires and increased aridity. However, water stress could convert forests into open shrublands by hampering post-fire recovery, with a possible tipping point at intermediate aridity. Projected increases in aridity may reduce the resilience of Mediterranean forests against fires and drive post-fire ecosystem dynamics toward open shrubland. The main effect of increased aridity is the limitation of post-fire recovery. Including plant fire-responses is thus fundamental when modelling the fate of Mediterranean-type vegetation under climate-change scenarios.

Grazing Away the Resilience of Patterned Ecosystems.

Ecosystems' responses to changing environmental conditions can be modulated by spatial self-organization. A prominent example of this can be found in drylands, where formation of vegetation patterns attenuates the magnitude of degradation events in response to decreasing rainfall. In model studies, the pattern wavelength responds to changing conditions, which is reflected by a rather gradual decline in biomass in response to decreasing rainfall. Although these models are spatially explicit, they have adopted a mean-field approach to grazing. By taking into account spatial variability when modeling grazing, we find that (over)grazing can lead to a dramatic shift in biomass, so that degradation occurs at rainfall rates that would otherwise still maintain a relatively productive ecosystem. Moreover, grazing increases the resilience of degraded ecosystem states. Consequently, restoration of degraded ecosystems could benefit from the introduction of temporary small-scale exclosures to escape from the basin of attraction of degraded states.

Catastrophic Shifts in Semiarid Vegetation-Soil Systems May Unfold Rapidly or Slowly.

Under gradual change of a driver, complex systems may switch between contrasting stable states. For many ecosystems it is unknown how rapidly such a critical transition unfolds. Here we explore the rate of change during the degradation of a semiarid ecosystem with a model coupling the vegetation and geomorphological system. Two stable states-vegetated and bare-are identified, and it is shown that the change between these states is a critical transition. Surprisingly, the critical transition between the vegetated and bare state can unfold either rapidly over a few years or gradually over decennia up to millennia, depending on parameter values. An important condition for the phenomenon is the linkage between slow and fast ecosystems components. Our results show that, next to climate change and disturbance rates, the geological and geomorphological setting of a semiarid ecosystem is crucial in predicting its fate.

Plant-plant interactions mediate the plastic and genotypic response of Plantago asiatica to CO2: an experiment with plant populations from naturally high CO2 areas.

BACKGROUND AND AIMS: The rising atmospheric CO2 concentration ([CO2]) is a ubiquitous selective force that may strongly impact species distribution and vegetation functioning. Plant-plant interactions could mediate the trajectory of vegetation responses to elevated [CO2], because some plants may benefit more from [CO2] elevation than others. The relative contribution of plastic (within the plant's lifetime) and genotypic (over several generations) responses to elevated [CO2] on plant performance was investigated and how these patterns are modified by plant-plant interactions was analysed. METHODS: Plantago asiatica seeds originating from natural CO2 springs and from ambient [CO2] sites were grown in mono stands of each one of the two origins as well as mixtures of both origins. In total, 1944 plants were grown in [CO2]-controlled walk-in climate rooms, under a [CO2] of 270, 450 and 750 ppm. A model was used for upscaling from leaf to whole-plant photosynthesis and for quantifying the influence of plastic and genotypic responses. KEY RESULTS: It was shown that changes in canopy photosynthesis, specific leaf area (SLA) and stomatal conductance in response to changes in growth [CO2] were mainly determined by plastic and not by genotypic responses. We further found that plants originating from high [CO2] habitats performed better in terms of whole-plant photosynthesis, biomass and leaf area, than those from ambient [CO2] habitats at elevated [CO2] only when both genotypes competed. Similarly, plants from ambient [CO2] habitats performed better at low [CO2], also only when both genotypes competed. No difference in performance was found in mono stands. CONCLUSION: The results indicate that natural selection under increasing [CO2] will be mainly driven by competitive interactions. This supports the notion that plant-plant interactions have an important influence on future vegetation functioning and species distribution. Furthermore, plant performance was mainly driven by plastic and not by genotypic responses to changes in atmospheric [CO2].

Phase separation explains a new class of self-organized spatial patterns in ecological systems.

The origin of regular spatial patterns in ecological systems has long fascinated researchers. Turing's activator-inhibitor principle is considered the central paradigm to explain such patterns. According to this principle, local activation combined with long-range inhibition of growth and survival is an essential prerequisite for pattern formation. Here, we show that the physical principle of phase separation, solely based on density-dependent movement by organisms, represents an alternative class of self-organized pattern formation in ecology. Using experiments with self-organizing mussel beds, we derive an empirical relation between the speed of animal movement and local animal density. By incorporating this relation in a partial differential equation, we demonstrate that this model corresponds mathematically to the well-known Cahn-Hilliard equation for phase separation in physics. Finally, we show that the predicted patterns match those found both in field observations and in our experiments. Our results reveal a principle for ecological self-organization, where phase separation rather than activation and inhibition processes drives spatial pattern formation.

Inhibitory and toxic effects of extracellular self-DNA in litter: a mechanism for negative plant-soil feedbacks?

Plant-soil negative feedback (NF) is recognized as an important factor affecting plant communities. The objectives of this work were to assess the effects of litter phytotoxicity and autotoxicity on root proliferation, and to test the hypothesis that DNA is a driver of litter autotoxicity and plant-soil NF. The inhibitory effect of decomposed litter was studied in different bioassays. Litter biochemical changes were evaluated with nuclear magnetic resonance (NMR) spectroscopy. DNA accumulation in litter and soil was measured and DNA toxicity was assessed in laboratory experiments. Undecomposed litter caused nonspecific inhibition of root growth, while autotoxicity was produced by aged litter. The addition of activated carbon (AC) removed phytotoxicity, but was ineffective against autotoxicity. Phytotoxicity was related to known labile allelopathic compounds. Restricted (13) C NMR signals related to nucleic acids were the only ones negatively correlated with root growth on conspecific substrates. DNA accumulation was observed in both litter decomposition and soil history experiments. Extracted total DNA showed evident species-specific toxicity. Results indicate a general occurrence of litter autotoxicity related to the exposure to fragmented self-DNA. The evidence also suggests the involvement of accumulated extracellular DNA in plant-soil NF. Further studies are needed to further investigate this unexpected function of extracellular DNA at the ecosystem level and related cellular and molecular mechanisms.

Inhibitory effects of extracellular self-DNA: a general biological process?

Self-inhibition of growth has been observed in different organisms, but an underlying common mechanism has not been proposed so far. Recently, extracellular DNA (exDNA) has been reported as species-specific growth inhibitor in plants and proposed as an explanation of negative plant-soil feedback. In this work the effect of exDNA was tested on different species to assess the occurrence of such inhibition in organisms other than plants. Bioassays were performed on six species of different taxonomic groups, including bacteria, fungi, algae, plants, protozoa and insects. Treatments consisted in the addition to the growth substrate of conspecific and heterologous DNA at different concentration levels. Results showed that treatments with conspecific DNA always produced a concentration dependent growth inhibition, which instead was not observed in the case of heterologous DNA. Reported evidence suggests the generality of the observed phenomenon which opens new perspectives in the context of self-inhibition processes. Moreover, the existence of a general species-specific biological effect of exDNA raises interesting questions on its possible involvement in self-recognition mechanisms. Further investigation at molecular level will be required to unravel the specific functioning of the observed inhibitory effects.

Cyclical succession in grazed ecosystems: the importance of interactions between different-sized herbivores and different-sized predators.

Body size of vertebrate herbivores is strongly linked to other life history traits, most notably (1) tolerance of low quality forage and (2) vulnerability to predation, which both impact the composition and dynamics of natural communities. However, no study has thus far explored how the combination of these two body-size related traits affects the long-term composition and dynamics of the herbivore and plant communities. We made a simple model of ordinary differential equations and simulated a grassland system with three herbivore species (small, medium, large) and two predator species (small, large) to investigate how the combination of low-quality tolerance and predation-vulnerability structure the herbivore and plant community. We found that facilitation and competition between different-sized herbivores and predation by especially small predators stimulate coexistence among herbivore species. Furthermore, the interaction between different-sized herbivores and predators generated cyclical succession in the plant community, i.e. alternating periods of short vegetation dominated by high-quality plants, with periods of tall vegetation dominated by low-quality plants. Our results suggest that cyclical succession in plant communities is more likely to occur when a predator predominantly preys on small herbivore species. Large predators also play an important role, as their addition relaxed the set of conditions under which cyclical succession occurred. Consequently, our model predictions suggest that a diverse predator community plays an important role in the long-term dynamics and maintenance of diversity in both the herbivore and plant community.

Early-warning signals for critical transitions.

Complex dynamical systems, ranging from ecosystems to financial markets and the climate, can have tipping points at which a sudden shift to a contrasting dynamical regime may occur. Although predicting such critical points before they are reached is extremely difficult, work in different scientific fields is now suggesting the existence of generic early-warning signals that may indicate for a wide class of systems if a critical threshold is approaching.

How light competition between plants affects their response to climate change.

How plants respond to climate change is of major concern, as plants will strongly impact future ecosystem functioning, food production and climate. Here, we investigated how vegetation structure and functioning may be influenced by predicted increases in annual temperatures and atmospheric CO2 concentration, and modeled the extent to which local plant-plant interactions may modify these effects. A canopy model was developed, which calculates photosynthesis as a function of light, nitrogen, temperature, CO2 and water availability, and considers different degrees of light competition between neighboring plants through canopy mixing; soybean (Glycine max) was used as a reference system. The model predicts increased net photosynthesis and reduced stomatal conductance and transpiration under atmospheric CO2 increase. When CO2 elevation is combined with warming, photosynthesis is increased more, but transpiration is reduced less. Intriguingly, when competition is considered, the optimal response shifts to producing larger leaf areas, but with lower stomatal conductance and associated vegetation transpiration than when competition is not considered. Furthermore, only when competition is considered are the predicted effects of elevated CO2 on leaf area index (LAI) well within the range of observed effects obtained by Free air CO2 enrichment (FACE) experiments. Together, our results illustrate how competition between plants may modify vegetation responses to climate change.

Facilitation and competition deconstructed: a mechanistic modelling approach to the stress gradient hypothesis applied to drylands.

Facilitative interactions among species are key in plant communities. While experimental tests support the Stress Gradient Hypothesis (SGH) as an association between facilitation and stress, whether the shape of net effects along stress gradients can be predicted is controversial, with no available mathematical modelling approaches. We proposed a novel test, using a modification of the R* model to study how negative and positive partial effects of plant interactions in drylands combine along two common stress gradients. We modelled different interactions: competition for water and light, amelioration of soil infiltration and/or grazing protection, obtaining that intensity and importance of facilitation did not generally increase along stress gradients, being dependent on the interaction type. While along the water stress gradient net interactions became more positive, reaching a maximum and then waning again, various outcomes were observed along the grazing gradient. Shape variety was mainly driven by the various shapes of the partial positive effects. Under resource stress, additive interaction effects can be expected, whereas when including grazing, the effects were non-additive. In the context of the SGH, deconstructing the effect of positive and negative interaction in a pairwise mechanistic models of drylands does not show a unique shape along stress gradients.

Travelling waves due to negative plant-soil feedbacks in a model including tree life-stages.

The emergence and maintenance of tree species diversity in tropical forests is commonly attributed to the Janzen-Connell (JC) hypothesis, which states that growth of seedlings is suppressed in the proximity of conspecific adult trees. As a result, a JC distribution due to a density-dependent negative feedback emerges in the form of a (transient) pattern where conspecific seedling density is highest at intermediate distances away from parent trees. Several studies suggest that the required density-dependent feedbacks behind this pattern could result from interactions between trees and soil-borne pathogens. However, negative plant-soil feedback may involve additional mechanisms, including the accumulation of autotoxic compounds generated through tree litter decomposition. An essential task therefore consists in constructing mathematical models incorporating both effects showing the ability to support the emergence of JC distributions. In this work, we develop and analyse a novel reaction-diffusion-ODE model, describing the interactions within tropical tree species across different life stages (seeds, seedlings, and adults) as driven by negative plant-soil feedback. In particular, we show that under strong negative plant-soil feedback travelling wave solutions exist, creating transient distributions of adult trees and seedlings that are in agreement with the Janzen-Connell hypothesis. Moreover, we show that these travelling wave solutions are pulled fronts and a robust feature as they occur over a broad parameter range. Finally, we calculate their linear spreading speed and show its (in)dependence on relevant nondimensional parameters.

A global analysis of how human infrastructure squeezes sandy coasts.

Coastal ecosystems provide vital services, but human disturbance causes massive losses. Remaining ecosystems are squeezed between rising seas and human infrastructure development. While shoreline retreat is intensively studied, coastal congestion through infrastructure remains unquantified. Here we analyse 235,469 transects worldwide to show that infrastructure occurs at a median distance of 392 meter from sandy shorelines. Moreover, we find that 33% of sandy shores harbour less than 100 m of infrastructure-free space, and that 23-30% of this space may be lost by 2100 due to rising sea levels. Further analyses show that population density and gross domestic product explain 35-39% of observed squeeze variation, emphasizing the intensifying pressure imposed as countries develop and populations grow. Encouragingly, we find that nature reserves relieve squeezing by 4-7 times. Yet, at present only 16% of world's sandy shores have a protected status. We therefore advocate the incorporation of nature protection into spatial planning policies.

Harnessing ecological theory to enhance ecosystem restoration.

Ecosystem restoration can increase the health and resilience of nature and humanity. As a result, the international community is championing habitat restoration as a primary solution to address the dual climate and biodiversity crises. Yet most ecosystem restoration efforts to date have underperformed, failed, or been burdened by high costs that prevent upscaling. To become a primary, scalable conservation strategy, restoration efficiency and success must increase dramatically. Here, we outline how integrating ten foundational ecological theories that have not previously received much attention - from hierarchical facilitation to macroecology - into ecosystem restoration planning and management can markedly enhance restoration success. We propose a simple, systematic approach to determining which theories best align with restoration goals and are most likely to bolster their success. Armed with a century of advances in ecological theory, restoration practitioners will be better positioned to more cost-efficiently and effectively rebuild the world's ecosystems and support the resilience of our natural resources.

Spatial vegetation patterns and imminent desertification in Mediterranean arid ecosystems.

Humans and climate affect ecosystems and their services, which may involve continuous and discontinuous transitions from one stable state to another. Discontinuous transitions are abrupt, irreversible and among the most catastrophic changes of ecosystems identified. For terrestrial ecosystems, it has been hypothesized that vegetation patchiness could be used as a signature of imminent transitions. Here, we analyse how vegetation patchiness changes in arid ecosystems with different grazing pressures, using both field data and a modelling approach. In the modelling approach, we extrapolated our analysis to even higher grazing pressures to investigate the vegetation patchiness when desertification is imminent. In three arid Mediterranean ecosystems in Spain, Greece and Morocco, we found that the patch-size distribution of the vegetation follows a power law. Using a stochastic cellular automaton model, we show that local positive interactions among plants can explain such power-law distributions. Furthermore, with increasing grazing pressure, the field data revealed consistent deviations from power laws. Increased grazing pressure leads to similar deviations in the model. When grazing was further increased in the model, we found that these deviations always and only occurred close to transition to desert, independent of the type of transition, and regardless of the vegetation cover. Therefore, we propose that patch-size distributions may be a warning signal for the onset of desertification.