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.

Habitat modification by marram grass negatively affects recruitment of conspecifics.

Ecosystem engineers alter their environment often benefiting their own survival and growth yielding self-reinforcing feedbacks. Moreover, these habitat modifications have been found to facilitate recruitment of conspecifics for some species, while for others engineering inhibits recruitment. Whether dune grasses facilitate or inhibit recruitment of conspecifics is yet unknown. Here, we investigated how habitat modification by European marram grass (Ammophila arenaria) through embryonic dune development affects recruitment from seeds and marine dispersed rhizome fragments. Specifically, we tested at three locations with different dune morphologies how habitat modification affected natural seed and rhizome presence and shoot emergence from plots in which seeds or rhizome fragments were added. In addition, we investigated how sediment burial (i.e., the main effect of habitat modification by dune grasses) affected germination and emergence in a controlled experiment. Results show that regardless of habitat modification or beach width, seeds and rhizomes were absent in natural conditions. Habitat modification negatively affected shoot emergence from seeds (8 × less) and rhizomes (4 × less) and was negatively related to sediment dynamics. Furthermore, fewer seedlings were found with higher elevations. In controlled laboratory conditions, the highest seedling emergence was found with slight burial (0.5-3 cm); both germination and seedling emergence decreased as seeds were buried deeper or shallower. Overall, habitat modification by marram grass negatively affects recruitment of conspecifics through increased sediment dynamics and elevation. Consequently, storm events or eradication programs that include removal of adult vegetation-which leads to an unmodified system-might benefit new recruitment from seeds or clonal fragments.

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.

The seafloor from a trait perspective. A comprehensive life history dataset of soft sediment macrozoobenthos.

Biological trait analysis (BTA) is a valuable tool for evaluating changes in community diversity and its link to ecosystem processes as well as environmental and anthropogenic perturbations. Trait-based analytical techniques like BTA rely on standardised datasets of species traits. However, there are currently only a limited number of datasets available for marine macrobenthos that contain trait data across multiple taxonomic groups. Here, we present an open-access dataset of 16 traits for 235 macrozoobenthic species recorded throughout multiple sampling campaigns of the Dutch Wadden Sea; a dynamic soft bottom system where humans have long played a substantial role in shaping the coastal environment. The trait categories included in this dataset cover a variety of life history strategies that are tightly linked to ecosystem functioning and the resilience of communities to (anthropogenic) perturbations and can advance our understanding of environmental changes and human impacts on the functioning of soft bottom systems.

Restoration ecology meets design-engineering: Mimicking emergent traits to restore feedback-driven ecosystems.

Ecosystems shaped by habitat-modifying organisms such as reefs, vegetated coastal systems and peatlands, provide valuable ecosystem services, such as carbon storage and coastal protection. However, they are declining worldwide. Ecosystem restoration is a key tool for mitigating these losses but has proven failure-prone, because ecosystem stability often hinges on self-facilitation generated by emergent traits from habitat modifiers. Emergent traits are not expressed by the single individual, but emerge at the level of an aggregation: a minimum patch-size or density-threshold must be exceeded to generate self-facilitation. Self-facilitation has been successfully harnessed for restoration by clumping transplanted organisms, but requires large amounts of often-limiting and costly donor material. Recent advancements highlight that kickstarting self-facilitation by mimicking emergent traits can similarly increase restoration success. Here, we provide a framework for combining expertise from ecologists, engineers and industrial product designers to transition from trial-and-error to emergent trait design-based, cost-efficient approaches to support large-scale restoration.

Early indicators of tidal ecosystem shifts in estuaries.

Forecasting transitions between tidal ecosystem states, such as between bare tidal flats and vegetated marshes, is crucial because it may imply the irreversible loss of valuable ecosystem services. In this study, we combine geospatial analyses of three European estuaries with a simple numerical model to demonstrate that the development of micro-topographic patterning on tidal flats is an early indicator of marsh establishment. We first show that the development of micro-topographic patterns precedes vegetation establishment, and that patterns tend to form only on tidal flats with a slope of <0.3 degrees. Numerical modelling then provides an explanation for the formation of micro-topography due to the natural concentration of draining surface water over very gentle slopes. We find this early indicator to be robust across three estuaries where anthropogenic deepening and narrowing has occurred in recent decades, which may suggest its broader applicability to other estuaries with similar morphological management.

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.

Recovering wetland biogeomorphic feedbacks to restore the world's biotic carbon hotspots.

Biogeomorphic wetlands cover 1% of Earth's surface but store 20% of ecosystem organic carbon. This disproportional share is fueled by high carbon sequestration rates and effective storage in peatlands, mangroves, salt marshes, and seagrass meadows, which greatly exceed those of oceanic and forest ecosystems. Here, we review how feedbacks between geomorphology and landscape-building vegetation underlie these qualities and how feedback disruption can switch wetlands from carbon sinks into sources. Currently, human activities are driving rapid declines in the area of major carbon-storing wetlands (1% annually). Our findings highlight the urgency to stop through conservation ongoing losses and to reestablish landscape-forming feedbacks through restoration innovations that recover the role of biogeomorphic wetlands as the world's biotic carbon hotspots.

Adaptive intertidal seed-based seagrass restoration in the Dutch Wadden Sea.

Seagrasses form the foundation of many coastal ecosystems but are rapidly declining on a global scale. The Dutch Wadden Sea once supported extensive subtidal seagrass meadows that have all disappeared. Here, we report on the setbacks and successes of intertidal seed-based restoration experiments in the Dutch Wadden Sea between 2014-2017. Our main goals were to 1) optimize plant densities, and 2) reduce seed losses. To achieve our goals, we conducted research-based, adaptive seagrass (Zostera marina) restoration, adjusting methods yearly based on previous results. We applied various seeding methods in three subsequent years-from Buoy Deployed Seeding (BuDS), and 'BuDS-in-frame' in fall, to a newly developed 'Dispenser Injection Seeding' (DIS) method. Our adaptive experimental approach revealed high seed losses between seeding and seedling establishment of the BuDS methods (>99.9%), which we mitigated by controlled harvest and storage of seeds throughout fall and winter, followed by DIS-seeding in spring. These iterative innovations resulted in 83 times higher plant densities in the field (0.012 to 1.00 plants m-2) and a small reduction in seed loss (99.94 to 99.75%) between 2015-2017. Although these developments have not yet resulted in self-sustaining seagrass populations, we are one step closer towards upscaling seagrass restoration in the Dutch Wadden Sea. Our outcomes suggest that an iterative, research-based restoration approach that focuses on technological advancement of precision-seeding may result in advancing knowledge and improved seed-based seagrass restoration successes.

Overcoming establishment thresholds for peat mosses in human-made bog pools.

Globally, peatlands have been affected by drainage and peat extraction, with adverse effects on their functioning and services. To restore peat-forming vegetation, drained bogs are being rewetted on a large scale. Although this practice results in higher groundwater levels, unfortunately it often creates deep lakes in parts where peat was extracted to greater depths than the surroundings. Revegetation of these deeper waters by peat mosses appears to be challenging due to strong abiotic feedbacks that keep these systems in an undesired bare state. In this study, we theoretically explore if a floating peat mat and an open human-made bog lake can be considered two alternative stable states using a simple model, and experimentally test in the field whether stable states are present, and whether a state shift can be accomplished using floating biodegradable structures that mimic buoyant peat. We transplanted two peat moss species into these structures (pioneer sp. Sphagnum cuspidatum and later-successional sp. S. palustre) with and without additional organic substrate. Our model suggests that these open human-made bog lakes and floating peat mats can indeed be regarded as alternative stable states. Natural recovery by spontaneous peat moss growth, i.e., a state shift from open water to floating mats, is only possible when the water table is sufficiently shallow to avoid light limitation (<0.29 m at our site). Our experiment revealed that alternative stable states are present and that the floating structures facilitated the growth of pioneer S. cuspidatum and vascular plants. Organic substrate addition particularly facilitated vascular plant growth, which correlated to higher moss height. The structures remained too wet for the late-successional species S. palustre. We conclude that open water and floating peat mats in human-made bog lakes can be considered two alternative stable states, and that temporary floating establishment structures can induce a state shift from the open water state to peat-forming vegetation state. These findings imply that for successful restoration, there is a clear water depth threshold to enable peat moss growth and there is no need for addition of large amounts of donor-peat substrate. Correct species selection for restoration is crucial for success.

Restoration of biogeomorphic systems by creating windows of opportunity to support natural establishment processes.

In degraded landscapes, recolonization by pioneer vegetation is often halted by the presence of persistent environmental stress. When natural expansion does occur, it is commonly due to the momentary alleviation of a key environmental variable previously limiting new growth. Thus, studying the circumstances in which expansion occurs can inspire new restoration techniques, wherein vegetation establishment is provoked by emulating natural events through artificial means. Using the salt-marsh pioneer zone on tidal flats as a biogeomorphic model system, we explore how locally raised sediment bed forms, which are the result of natural (bio)geomorphic processes, enhance seedling establishment in an observational study. We then conduct a manipulative experiment designed to emulate these facilitative conditions in order to enable establishment on an uncolonized tidal flat. Here, we attempt to generate raised growth-promoting sediment bed forms using porous artificial structures. Flume experiments demonstrate how these structures produce a sheltered hydrodynamic environment in which suspended sediment and seeds preferentially settle. The application of these structures in the field led to the formation of stable, raised sediment platforms and the spontaneous recruitment of salt-marsh pioneers in the following growing season. These recruits were composed primarily of the annual pioneering Salicornia genus, with densities of up to 140 individuals/m2 within the structures, a 60-fold increase over ambient densities. Lower abundances of five other perennial species were found within structures that did not appear elsewhere in the pioneer zone. Furthermore, recruits grew to be on average three times greater in mass inside of the structures than in the neighboring ambient environment. The success of this restoration design may be attributed to the combination of three factors: (1) enhanced seed retention, (2) suppressed mortality, and (3) accelerated growth rates on the elevated surfaces generated by the artificial structures. We argue that restoration approaches similar to the one shown here, wherein the conditions for natural establishment are actively mimicked to promote vegetation development, may serve as promising tools in many biogeomorphic ecosystems, ranging from coastal to arid ecosystems.

Saltmarsh resilience controlled by patch size and plant density of habitat-forming species that trap shells.

Habitat fragmentaion into small patches is regarded as a vital cause of biodiversity loss. Fragmentationof habitat-forming species is especially harmful, as patchiness of such species often controls ecosystem stability and resilience by density and patch size-dependent self-reinforcing feedbacks. Although fragmentation are expected to weaken or even break such feedbacks, it remains unclear how the resulting patchiness of habitat-forming species affect ecosystem resilience to environmental stresses. Here, using Spartian alterniflora, the habitat-forming species in saltmarshes as a model, we investigate how patch size, plant density, and shell aggregation interactively control the persistence of a degrading salt marsh that suffered from erosion induced by hydrodynamics. Our results demonstrate that large patches can trap more shells along the patch edge than the smaller ones, therefore significantly facilitating plant re-growth within the patch. Shell removal experiments further reveal that large patches trapping more shells along patch edges reinforce their own persistence by decreasing erosion and thus facilitating plant recovery. By contrast, small patches with lesser plants cannot persist as they trap less shells along patch edges but are able to accumulate more shells at interior locations where they hinder plant re-growth, indicating a critical threshold of patch size ~20 m2 below which ecosystem collapses. The current study highlights the importance to identify critical threshold of stress-resistant patch sizes in transition-prone ecosystems as early-warning to alert undesired ecosystem collapse and restoration practice.

Facultative mutualisms: A double-edged sword for foundation species in the face of anthropogenic global change.

Ecosystems worldwide depend on habitat-forming foundation species that often facilitate themselves with increasing density and patch size, while also engaging in facultative mutualisms. Anthropogenic global change (e.g., climate change, eutrophication, overharvest, land-use change), however, is causing rapid declines of foundation species-structured ecosystems, often typified by sudden collapse. Although disruption of obligate mutualisms involving foundation species is known to precipitate collapse (e.g., coral bleaching), how facultative mutualisms (i.e., context-dependent, nonbinding reciprocal interactions) affect ecosystem resilience is uncertain. Here, we synthesize recent advancements and combine these with model analyses supported by real-world examples, to propose that facultative mutualisms may pose a double-edged sword for foundation species. We suggest that by amplifying self-facilitative feedbacks by foundation species, facultative mutualisms can increase foundation species' resistance to stress from anthropogenic impact. Simultaneously, however, mutualism dependency can generate or exacerbate bistability, implying a potential for sudden collapse when the mutualism's buffering capacity is exceeded, while recovery requires conditions to improve beyond the initial collapse point (hysteresis). Thus, our work emphasizes the importance of acknowledging facultative mutualisms for conservation and restoration of foundation species-structured ecosystems, but highlights the potential risk of relying on mutualisms in the face of global change. We argue that significant caveats remain regarding the determination of these feedbacks, and suggest empirical manipulation across stress gradients as a way forward to identify related nonlinear responses.

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.

Mimicry of emergent traits amplifies coastal restoration success.

Restoration is becoming a vital tool to counteract coastal ecosystem degradation. Modifying transplant designs of habitat-forming organisms from dispersed to clumped can amplify coastal restoration yields as it generates self-facilitation from emergent traits, i.e. traits not expressed by individuals or small clones, but that emerge in clumped individuals or large clones. Here, we advance restoration science by mimicking key emergent traits that locally suppress physical stress using biodegradable establishment structures. Experiments across (sub)tropical and temperate seagrass and salt marsh systems demonstrate greatly enhanced yields when individuals are transplanted within structures mimicking emergent traits that suppress waves or sediment mobility. Specifically, belowground mimics of dense root mats most facilitate seagrasses via sediment stabilization, while mimics of aboveground plant structures most facilitate marsh grasses by reducing stem movement. Mimicking key emergent traits may allow upscaling of restoration in many ecosystems that depend on self-facilitation for persistence, by constraining biological material requirements and implementation costs.

Resilience of beach grasses along a biogeomorphic successive gradient: resource availability vs. clonal integration.

Coastal ecosystems are often formed through two-way interactions between plants and their physical landscape. By expanding clonally, landscape-forming plants can colonize bare unmodified environments and stimulate vegetation-landform feedback interactions. Yet, to what degree these plants rely on clonal integration for overcoming physical stress during biogeomorphological succession remains unknown. Here, we investigated the importance of clonal integration and resource availability on the resilience of two European beach grasses (i.e. Elytrigia juncea and Ammophila arenaria) over a natural biogeomorphic dune gradient from beach (unmodified system) to foredune (biologically modified system). We found plant resilience, as measured by its ability to recover and expand following disturbance (i.e. plant clipping), to be independent on the presence of rhizomal connections between plant parts. Instead, resource availability over the gradient largely determined plant resilience. The pioneer species, Elytrigia, demonstrated a high resilience to physical stress, independent of its position on the biogeomorphic gradient (beach or embryonic dune). In contrast, the later successional species (Ammophila) proved to be highly resilient on the lower end of its distribution (embryonic dune), but it did not fully recover on the foredunes, most likely as a result of nutrient deprivation. We argue that in homogenously resource-poor environments as our beach system, overall resource availability, instead of translocation through a clonal network, determines the resilience of plant species. Hence, the formation of high coastal dunes may increase the resistance of beach grasses to the physical stresses of coastal flooding, but the reduced marine nutrient input may negatively affect the resilience of plants.

Nutrient availability induces community shifts in seagrass meadows grazed by turtles.

In the Caribbean, green turtles graze seagrass meadows dominated by Thalassia testudinum through rotational grazing, resulting in the creation of grazed and recovering (abandoned) patches surrounded by ungrazed seagrasses. We evaluated the seagrass community and its environment along a turtle grazing gradient; with the duration of (simulated) grazing as a proxy for the level of grazing pressure. The grazing levels consisted of Short-term (4 months clipping), Medium-term (8 months clipping), Long-term grazing (8 months of clipping in previously grazed areas), 8-months recovery of previously grazed patches, and ungrazed or unclipped patches as controls. We measured biomass and density of the seagrasses and rhizophytic algae, and changes in sediment parameters. Medium- and Long-term grazing promoted a shift in community species composition. At increasing grazing pressure, the total biomass of T. testudinum declined, whereas that of early-successional increased. Ammonium concentrations were highest in the patches of Medium-term (9.2 + 0.8 µM) and Long-term grazing levels (11.0 + 2.2 µM) and were lowest in the control areas (4.6 + 1.5 µM). T. testudinum is a late-successional species that maintains sediment nutrient concentrations at levels below the requirements of early-successional species when dominant. When the abundance of this species declines due to grazing, these resources become available, likely driving a shift in community composition toward a higher abundance of early-successional species.

A Lévy expansion strategy optimizes early dune building by beach grasses.

Lifeforms ranging from bacteria to humans employ specialized random movement patterns. Although effective as optimization strategies in many scientific fields, random walk application in biology has remained focused on search optimization by mobile organisms. Here, we report on the discovery that heavy-tailed random walks underlie the ability of clonally expanding plants to self-organize and dictate the formation of biogeomorphic landscapes. Using cross-Atlantic surveys, we show that congeneric beach grasses adopt distinct heavy-tailed clonal expansion strategies. Next, we demonstrate with a spatially explicit model and a field experiment that the Lévy-type strategy of the species building the highest dunes worldwide generates a clonal network with a patchy shoot organization that optimizes sand trapping efficiency. Our findings demonstrate Lévy-like movement in plants, and emphasize the role of species-specific expansion strategies in landscape formation. This mechanistic understanding paves the way for tailor-made planting designs to successfully construct and restore biogeomorphic landscapes and their services.

Foundation species enhance food web complexity through non-trophic facilitation.

Food webs are an integral part of every ecosystem on the planet, yet understanding the mechanisms shaping these complex networks remains a major challenge. Recently, several studies suggested that non-trophic species interactions such as habitat modification and mutualisms can be important determinants of food web structure. However, it remains unclear whether these findings generalize across ecosystems, and whether non-trophic interactions affect food webs randomly, or affect specific trophic levels or functional groups. Here, we combine analyses of 58 food webs from seven terrestrial, freshwater and coastal systems to test (1) the general hypothesis that non-trophic facilitation by habitat-forming foundation species enhances food web complexity, and (2) whether these enhancements have either random or targeted effects on particular trophic levels, functional groups, and linkages throughout the food web. Our empirical results demonstrate that foundation species consistently enhance food web complexity in all seven ecosystems. Further analyses reveal that 15 out of 19 food web properties can be well-approximated by assuming that foundation species randomly facilitate species throughout the trophic network. However, basal species are less strongly, and carnivores are more strongly facilitated in foundation species' food webs than predicted based on random facilitation, resulting in a higher mean trophic level and a longer average chain length. Overall, we conclude that foundation species strongly enhance food web complexity through non-trophic facilitation of species across the entire trophic network. We therefore suggest that the structure and stability of food webs often depends critically on non-trophic facilitation by foundation species.

A facultative mutualistic feedback enhances the stability of tropical intertidal seagrass beds.

Marine foundation species such as corals, seagrasses, salt marsh plants, and mangrove trees are increasingly found to engage in mutualistic interactions. Because mutualisms by their very nature generate a positive feedback between the species, subtle environmental impacts on one of the species involved may trigger mutualism breakdown, potentially leading to ecosystem regime shifts. Using an empirically parameterized model, we investigate a facultative mutualism between seagrass and lucinid bivalves with endosymbiotic sulfide-oxidizing gill bacteria in a tropical intertidal ecosystem. Model predictions for our system show that, by alleviating the build-up of toxic sulfide, this mutualism maintains an otherwise intrinsically unstable seagrass ecosystem. However, an increase in seagrass mortality above natural levels, due to e.g. desiccation stress, triggers mutualism breakdown. This pushes the system in collapse-and-recovery dynamics ('slow-fast cycles') characterized by long-term persistent states of bare and seagrass-dominated, with rapid transitions in between. Model results were consistent with remote sensing analyses that suggest feedback-mediated state shifts induced by desiccation. Overall, our combined theoretical and empirical results illustrate the potential of mutualistic feedbacks to stabilize ecosystems, but also reveal an important drawback as small environmental changes may trigger shifts. We therefore suggest that mutualisms should be considered for marine conservation and restoration of seagrass beds.