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.

Long-distance facilitation of coastal ecosystem structure and resilience.

Biotic interactions that hierarchically organize ecosystems by driving ecological and evolutionary processes across spatial scales are ubiquitous in our biosphere. Biotic interactions have been extensively studied at local and global scales, but how long-distance, cross-ecosystem interactions at intermediate landscape scales influence the structure, function, and resilience of ecological systems remains poorly understood. We used remote sensing, modeling, and field data to test the hypothesis that the long-distance impact of an invasive species dramatically affects one of the largest tidal flat ecosystems in East Asia. We found that the invasion of exotic cordgrass Spartina alterniflora can produce long-distance effects on native species up to 10 km away, driving decadal coastal ecosystem transitions. The invasive cordgrass at low elevations facilitated the expansion of the native reed Phragmites australis at high elevations, leading to the massive loss and reduced resilience of the iconic Suaeda salsa "Red Beach" marshes at intermediate elevations, largely as a consequence of reduced soil salinity across the landscape. Our results illustrate the complex role that long-distance interactions can play in shaping landscape structure and ecosystem resilience and in bridging the gap between local and global biotic interactions.

Ice needles weave patterns of stones in freezing landscapes.

Patterned ground, defined by the segregation of stones in soil according to size, is one of the most strikingly self-organized characteristics of polar and high-alpine landscapes. The presence of such patterns on Mars has been proposed as evidence for the past presence of surface liquid water. Despite their ubiquity, the dearth of quantitative field data on the patterns and their slow dynamics have hindered fundamental understanding of the pattern formation mechanisms. Here, we use laboratory experiments to show that stone transport is strongly dependent on local stone concentration and the height of ice needles, leading effectively to pattern formation driven by needle ice activity. Through numerical simulations, theory, and experiments, we show that the nonlinear amplification of long wavelength instabilities leads to self-similar dynamics that resemble phase separation patterns in binary alloys, characterized by scaling laws and spatial structure formation. Our results illustrate insights to be gained into patterns in landscapes by viewing the pattern formation through the lens of phase separation. Moreover, they may help interpret spatial structures that arise on diverse planetary landscapes, including ground patterns recently examined using the rover Curiosity on Mars.

Sediment availability provokes a shift from Brownian to Lévy-like clonal expansion in a dune building grass.

In biogeomorphic landscapes, plant traits can steer landscape development through plant-mediated feedback interactions. Interspecific differences in clonal expansion strategy can therefore lead to the emergence of different landscape organisations. Yet, whether landscape-forming plants adopt different clonal expansion strategies depending on their physical environment remains to be tested. Here, we use a field survey and a complementary mesocosm approach to investigate whether sediment deposition affects the clonal expansion strategy employed by dune-building marram grass individuals. Our results reveal a consistent shift in expansion pattern from more clumped, Brownian-like, movement in sediment-poor conditions, to patchier, Lévy-like, movement under high sediment supply rates. Additional model simulations illustrate that the sediment-dependent shift in movement strategies induces a shift in optimisation of the cost-benefit relation between landscape engineering (i.e. dune formation) and expansion. Plasticity in expansion strategy may therefore allow landscape-forming plants to optimise their engineering ability depending on their physical landscape.

Density-Dependent and Species-Specific Effects on Self-Organization Modulate the Resistance of Mussel Bed Ecosystems to Hydrodynamic Stress.

AbstractSelf-organized, regular spatial patterns emerging from local interactions among individuals enhance the ability of ecosystems to respond to environmental disturbances. Mussels self-organize to form large, regularly patterned biogenic structures that modify the biotic and abiotic environment and provide numerous ecosystem functions and services. We used two mussel species that form monospecific and mixed beds to investigate how species-specific behavior affects self-organization and resistance to wave stress. Perna perna has strong attachment but low motility, while Mytilus galloprovincialis shows the reverse. At low density, the less motile P. perna has limited spatial self-organization compared with M. galloprovincialis, while when coexisting, the two species formed random spatial patterns. At high density, the two species self-organized in similar ways, while when coexisting, patterns were less strong. Spatial pattern formations significantly shaped resistance to hydrodynamic stress. At low density, P. perna beds with strong attachment and M. galloprovincialis beds with strong spatial organization showed higher retention rates than mixed beds. At high density, the presence of strongly attached P. perna significantly increased retention in mixed and P. perna beds compared with M. galloprovincialis beds. Our study emphasizes the importance of the interplay of species-specific behaviors to spatial self-organization and stress tolerance in natural communities.

A Comparison of the "Reduced Losses" and "Increased Production" Models for Mussel Bed Dynamics.

Self-organised regular pattern formation is one of the foremost examples of the development of complexity in ecosystems. Despite the wide array of mechanistic models that have been proposed to understand pattern formation, there is limited general understanding of the feedback processes causing pattern formation in ecosystems, and how these affect ecosystem patterning and functioning. Here we propose a generalised model for pattern formation that integrates two types of within-patch feedback: amplification of growth and reduction of losses. Both of these mechanisms have been proposed as causing pattern formation in mussel beds in intertidal regions, where dense clusters of mussels form, separated by regions of bare sediment. We investigate how a relative change from one feedback to the other affects the stability of uniform steady states and the existence of spatial patterns. We conclude that there are important differences between the patterns generated by the two mechanisms, concerning both biomass distribution in the patterns and the resilience of the ecosystems to disturbances.

Self-organization of river vegetation leads to emergent buffering of river flows and water levels.

Global climate change is expected to impact hydrodynamic conditions in stream ecosystems. There is limited understanding of how stream ecosystems interact and possibly adapt to novel hydrodynamic conditions. Combining mathematical modelling with field data, we demonstrate that bio-physical feedback between plant growth and flow redistribution triggers spatial self-organization of in-channel vegetation that buffers for changed hydrological conditions. The interplay of vegetation growth and hydrodynamics results in a spatial separation of the stream into densely vegetated, low-flow zones divided by unvegetated channels of higher flow velocities. This self-organization process decouples both local flow velocities and water levels from the forcing effect of changing stream discharge. Field data from two lowland, baseflow-dominated streams support model predictions and highlight two important stream-level emergent properties: vegetation controls flow conveyance in fast-flowing channels throughout the annual growth cycle, and this buffering of discharge variations maintains water depths and wetted habitat for the stream community. Our results provide important evidence of how plant-driven self-organization allows stream ecosystems to adapt to changing hydrological conditions, maintaining suitable hydrodynamic conditions to support high biodiversity.

Behavioral self-organization underlies the resilience of a coastal ecosystem.

Self-organized spatial patterns occur in many terrestrial, aquatic, and marine ecosystems. Theoretical models and observational studies suggest self-organization, the formation of patterns due to ecological interactions, is critical for enhanced ecosystem resilience. However, experimental tests of this cross-ecosystem theory are lacking. In this study, we experimentally test the hypothesis that self-organized pattern formation improves the persistence of mussel beds (Mytilus edulis) on intertidal flats. In natural beds, mussels generate self-organized patterns at two different spatial scales: regularly spaced clusters of mussels at centimeter scale driven by behavioral aggregation and large-scale, regularly spaced bands at meter scale driven by ecological feedback mechanisms. To test for the relative importance of these two spatial scales of self-organization on mussel bed persistence, we conducted field manipulations in which we factorially constructed small-scale and/or large-scale patterns. Our results revealed that both forms of self-organization enhanced the persistence of the constructed mussel beds in comparison to nonorganized beds. Small-scale, behaviorally driven cluster patterns were found to be crucial for persistence, and thus resistance to wave disturbance, whereas large-scale, self-organized patterns facilitated reformation of small-scale patterns if mussels were dislodged. This study provides experimental evidence that self-organization can be paramount to enhancing ecosystem persistence. We conclude that ecosystems with self-organized spatial patterns are likely to benefit greatly from conservation and restoration actions that use the emergent effects of self-organization to increase ecosystem resistance to disturbance.

The shaping role of self-organization: linking vegetation patterning, plant traits and ecosystem functioning.

Self-organized spatial patterns are increasingly recognized for their contribution to ecosystem functioning, in terms of enhanced productivity, ecosystem stability, and species diversity in terrestrial as well as marine ecosystems. Most studies on the impact of spatial self-organization have focused on systems that exhibit regular patterns. However, there is an abundance of patterns in many ecosystems which are not strictly regular. Understanding of how these patterns are formed and how they affect ecosystem function is crucial for the broad acceptance of self-organization as a keystone process in ecological theory. Here, using transplantation experiments in salt marsh ecosystems dominated by Scirpus mariqueter, we demonstrate that scale-dependent feedback is driving irregular spatial pattern formation of vegetation. Field observations and experiments have revealed that this self-organization process affects a range of plant traits, including shoot-to-root ratio, rhizome orientation, rhizome node number, and rhizome length, and enhances vegetation productivity. Moreover, patchiness in self-organized salt marsh vegetation can support a better microhabitat for macrobenthos, promoting their total abundance and spatial heterogeneity of species richness. Our results extend existing concepts of self-organization and its effects on productivity and biodiversity to the spatial irregular patterns that are observed in many systems. Our work also helps to link between the so-far largely unconnected fields of self-organization theory and trait-based, functional ecology.

Weather fluctuations affect the impact of consumers on vegetation recovery following a catastrophic die-off.

Prolonged droughts exacerbated by climate change have been widely documented to interact with consumers to decimate vegetation in many ecosystems. Although climate change is increasing within-year variation in precipitation and temperature, how weather fluctuations affect the impact of consumers on vegetation processes remains poorly understood. In a salt marsh that has recently experienced drought-associated vegetation die-off, we investigated how top-down control of plant recovery by a prominent salt marsh grazer varies with weather. Our results showed that grazing-driven plant mortality varied strongly with weather in spring, with intense grazing occurring during cool, wet days immediately following rain. Intense grazing on cool, wet days across the generally dry spring season had a strong impact that eliminated plant seedlings that could otherwise have become tolerant of grazing in the following summer, thereby restricting vegetation recovery and contributing to the persistence of an unvegetated salt barren state. Thus, weather fluctuations can modulate the impact of consumers on vegetation recovery, a fundamental process underlying the fate of ecosystems after disturbances. A multi-timescale perspective on top-down control that combines the impact of short-term fluctuations in weather and that of long-term variation in mean climate can not only help understand ecosystem dynamics in an increasingly variable climate, but may also inform conservation strategies or recovery plans for ecosystems that are already lost to climate change.

Landscapes of facilitation: how self-organized patchiness of aquatic macrophytes promotes diversity in streams.

Spatial heterogeneity plays a crucial role in the coexistence of species. Despite recognition of the importance of self-organization in creating environmental heterogeneity in otherwise uniform landscapes, the effects of such self-organized pattern formation in promoting coexistence through facilitation are still unknown. In this study, we investigated the effects of pattern formation on species interactions and community spatial structure in ecosystems with limited underlying environmental heterogeneity, using self-organized patchiness of the aquatic macrophyte Callitriche platycarpa in streams as a model system. Our theoretical model predicted that pattern formation in aquatic vegetation - due to feedback interactions between plant growth, water flow and sedimentation processes - could promote species coexistence, by creating heterogeneous flow conditions inside and around the plant patches. The spatial plant patterns predicted by our model agreed with field observations at the reach scale in naturally vegetated rivers, where we found a significant spatial aggregation of two macrophyte species around C. platycarpa. Field transplantation experiments showed that C. platycarpa had a positive effect on the growth of both beneficiary species, and the intensity of this facilitative effect was correlated with the heterogeneous hydrodynamic conditions created within and around C. platycarpa patches. Our results emphasize the importance of self-organized patchiness in promoting species coexistence by creating a landscape of facilitation, where new niches and facilitative effects arise in different locations. Understanding the interplay between competition and facilitation is therefore essential for successful management of biodiversity in many ecosystems.

Facilitation shifts paradigms and can amplify coastal restoration efforts.

Restoration has been elevated as an important strategy to reverse the decline of coastal wetlands worldwide. Current practice in restoration science emphasizes minimizing competition between out-planted propagules to maximize planting success. This paradigm persists despite the fact that foundational theory in ecology demonstrates that positive species interactions are key to organism success under high physical stress, such as recolonization of bare substrate. As evidence of how entrenched this restoration paradigm is, our survey of 25 restoration organizations in 14 states in the United States revealed that >95% of these agencies assume minimizing negative interactions (i.e., competition) between outplants will maximize propagule growth. Restoration experiments in both Western and Eastern Atlantic salt marshes demonstrate, however, that a simple change in planting configuration (placing propagules next to, rather than at a distance from, each other) results in harnessing facilitation and increased yields by 107% on average. Thus, small adjustments in restoration design may catalyze untapped positive species interactions, resulting in significantly higher restoration success with no added cost. As positive interactions between organisms commonly occur in coastal ecosystems (especially in more physically stressful areas like uncolonized substrate) and conservation resources are limited, transformation of the coastal restoration paradigm to incorporate facilitation theory may enhance conservation efforts, shoreline defense, and provisioning of ecosystem services such as fisheries production.

How habitat-modifying organisms structure the food web of two coastal ecosystems.

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.

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.

Experimental evidence for inherent Lévy search behaviour in foraging animals.

Recently, Lévy walks have been put forward as a new paradigm for animal search and many cases have been made for its presence in nature. However, it remains debated whether Lévy walks are an inherent behavioural strategy or emerge from the animal reacting to its habitat. Here, we demonstrate signatures of Lévy behaviour in the search movement of mud snails (Hydrobia ulvae) based on a novel, direct assessment of movement properties in an experimental set-up using different food distributions. Our experimental data uncovered clusters of small movement steps alternating with long moves independent of food encounter and landscape complexity. Moreover, size distributions of these clusters followed truncated power laws. These two findings are characteristic signatures of mechanisms underlying inherent Lévy-like movement. Thus, our study provides clear experimental evidence that such multi-scale movement is an inherent behaviour rather than resulting from the animal interacting with its environment.

Degradation and resilience in Louisiana salt marshes after the BP-Deepwater Horizon oil spill.

More than 2 y have passed since the BP-Deepwater Horizon oil spill in the Gulf of Mexico, yet we still have little understanding of its ecological impacts. Examining effects of this oil spill will generate much-needed insight into how shoreline habitats and the valuable ecological services they provide (e.g., shoreline protection) are affected by and recover from large-scale disturbance. Here we report on not only rapid salt-marsh recovery (high resilience) but also permanent marsh area loss after the BP-Deepwater Horizon oil spill. Field observations, experimental manipulations, and wave-propagation modeling reveal that (i) oil coverage was primarily concentrated on the seaward edge of marshes; (ii) there were thresholds of oil coverage that were associated with severity of salt-marsh damage, with heavy oiling leading to plant mortality; (iii) oil-driven plant death on the edges of these marshes more than doubled rates of shoreline erosion, further driving marsh platform loss that is likely to be permanent; and (iv) after 18 mo, marsh grasses have largely recovered into previously oiled, noneroded areas, and the elevated shoreline retreat rates observed at oiled sites have decreased to levels at reference marsh sites. This paper highlights that heavy oil coverage on the shorelines of Louisiana marshes, already experiencing elevated retreat because of intense human activities, induced a geomorphic feedback that amplified this erosion and thereby set limits to the recovery of otherwise resilient vegetation. It thus warns of the enhanced vulnerability of already degraded marshes to heavy oil coverage and provides a clear example of how multiple human-induced stressors can interact to hasten ecosystem decline.

How superdiffusion gets arrested: ecological encounters explain shift from Lévy to Brownian movement.

Ecological theory uses Brownian motion as a default template for describing ecological movement, despite limited mechanistic underpinning. The generality of Brownian motion has recently been challenged by empirical studies that highlight alternative movement patterns of animals, especially when foraging in resource-poor environments. Yet, empirical studies reveal animals moving in a Brownian fashion when resources are abundant. We demonstrate that Einstein's original theory of collision-induced Brownian motion in physics provides a parsimonious, mechanistic explanation for these observations. Here, Brownian motion results from frequent encounters between organisms in dense environments. In density-controlled experiments, movement patterns of mussels shifted from Lévy towards Brownian motion with increasing density. When the analysis was restricted to moves not truncated by encounters, this shift did not occur. Using a theoretical argument, we explain that any movement pattern approximates Brownian motion at high-resource densities, provided that movement is interrupted upon encounters. Hence, the observed shift to Brownian motion does not indicate a density-dependent change in movement strategy but rather results from frequent collisions. Our results emphasize the need for a more mechanistic use of Brownian motion in ecology, highlighting that especially in rich environments, Brownian motion emerges from ecological interactions, rather than being a default movement pattern.

Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas.

Marine protected areas (MPAs) are key tools for combatting the global overexploitation of endangered species. The prevailing paradigm is that MPAs are beneficial in helping to restore ecosystems to more 'natural' conditions. However, MPAs may have unintended negative effects when increasing densities of protected species exert destructive effects on their habitat. Here, we report on severe seagrass degradation in a decade-old MPA where hyper-abundant green turtles adopted a previously undescribed below-ground foraging strategy. By digging for and consuming rhizomes and roots, turtles create abundant bare gaps, thereby enhancing erosion and reducing seagrass regrowth. A fully parametrized model reveals that the ecosystem is approaching a tipping point, where consumption overwhelms regrowth, which could potentially lead to complete collapse of the seagrass habitat. Seagrass recovery will not ensue unless turtle density is reduced to nearly zero, eliminating the MPA's value as a turtle reserve. Our results reveal an unrecognized, yet imminent threat to MPAs, as sea turtle densities are increasing at major nesting sites and the decline of seagrass habitat forces turtles to concentrate on the remaining meadows inside reserves. This emphasizes the need for policy and management approaches that consider the interactions of protected species with their habitat.

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.

Cross-habitat interactions among bivalve species control community structure on intertidal flats.

Increasing evidence shows that spatial interactions between sedentary organisms can structure communities and promote landscape complexity in many ecosystems. Here we tested the hypothesis that reef-forming mussels (Mytilus edulis L.), a dominant intertidal ecosystem engineer in the Wadden Sea, promote abundances of the burrowing bivalve Cerastoderma edule L. (cockle) in neighboring habitats at relatively long distances coastward from mussel beds. Field surveys within and around three mussel beds showed a peak in cockle densities at 50-100 m toward the coast from the mussel bed, while cockle abundances elsewhere in the study area were very low. Field transplantation of cockles showed higher survival of young cockles (2-3 years old) and increased spat fall coastward of the mussel bed compared to within the bed and to areas without mussels, whereas growth decreased within and coastward of the mussel bed. Our measurements suggest that the observed spatial patterns in cockle numbers resulted from (1) inhibition effects by the mussels close to the beds due to preemptive algal depletion and deteriorated sediment conditions and (2) facilitation effects by the mussels farther away from the beds due to reduction of wave energy. Our results imply that these spatial, scale-dependent interactions between reef-forming ecosystem engineers and surrounding communities of sedentary benthic organisms can be an important determinant of the large-scale community structure in intertidal ecosystems. Understanding this interplay between neighboring communities of sedentary species is therefore essential for effective conservation and restoration of soft-bottom intertidal communities.