Wave effects on seedling establishment of three pioneer marsh species: survival, morphology and biomechanics.

BACKGROUND AND AIMS: It is important to have an in-depth mechanistic understanding of tidal marsh establishment and dynamics to ensure the long-term persistence of these valuable ecosystems. As wave forcing may be expected to impact seedling establishment, we studied the effect of water-imposed drag forces on seedling survival, morphology and biomechanical properties of three marsh pioneer species that are dominant along the salinity gradient in many areas around the world: Spartina anglica (salt to brackish), Scirpus maritimus (brackish) and Phragmites australis (brackish to fresh). METHODS: Using a newly developed plant-shaking mesocosm (PSM) that mimicked water-imposed wave drag forces, the effect of wave stress on seedling survival was examined, together with impacts on morphology and biomechanical properties. KEY RESULTS: After 7 weeks of exposure to wave stress, lowered seedling survival and growth for all species was revealed. Wave treatments increased the root/shoot biomass ratio to enhance anchorage and made seedlings more flexible (i.e. reduced flexural rigidity), which might be regarded as a mixed outcome between a stress avoidance and stress tolerance strategy. CONCLUSIONS: The different biomechanical responses between the three dominant marsh pioneer species, overall, make them less resistant to external stress. Therefore, our results indicate that the likelihood of marshes becoming established is reduced if wave energy increases. Despite the different biomechanical response of these three pioneer species to waves, the seedlings of all species were found to have low resistance to external stresses.

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.

Ecosystem engineering creates a new path to resilience in plants with contrasting growth strategies.

Plant species can be characterized by different growth strategies related to their inherent growth and recovery rates, which shape their responses to stress and disturbance. Ecosystem engineering, however, offers an alternative way to cope with stress: modifying the environment may reduce stress levels. Using an experimental study on two seagrass species with contrasting traits, the slow-growing Zostera marina vs. the fast-growing Zostera japonica, we explored how growth strategies versus ecosystem engineering may affect their resistance to stress (i.e. addition of organic material) and recovery from disturbance (i.e. removal of above-ground biomass). Ecosystem engineering was assessed by measuring sulphide levels in the sediment porewater, as seagrass plants can keep sulphide levels low by aerating the rhizosphere. Consistent with predictions, we observed that the fast-growing species had a high capacity to recover from disturbance. It was also more resistant to stress and still able to maintain high standing stock with increasing stress levels because of its ecosystem engineering capacity. The slow-growing species was not able to maintain its standing stock under stress, which we ascribe to a weak capacity for ecosystem engineering regarding this particular stress. Overall, our study suggests that the combination of low-cost investment in tissues with ecosystem engineering to alleviate stress creates a new path in the growth trade-off between investment in strong tissues or fast growth. It does so by being both fast in recovery and more resistant. As such low-cost ecosystem engineering may occur in more species, we argue that it should be considered in assessing plant resilience.

Ecosystem-based coastal defence in the face of global change.

The risk of flood disasters is increasing for many coastal societies owing to global and regional changes in climate conditions, sea-level rise, land subsidence and sediment supply. At the same time, in many locations, conventional coastal engineering solutions such as sea walls are increasingly challenged by these changes and their maintenance may become unsustainable. We argue that flood protection by ecosystem creation and restoration can provide a more sustainable, cost-effective and ecologically sound alternative to conventional coastal engineering and that, in suitable locations, it should be implemented globally and on a large scale.

Sprouting as a gardening strategy to obtain superior supplementary food: evidence from a seed-caching marine worm.

Only a handful of non-human animals are known to grow their own food by cultivating high-yield fungal or algal crops as staple food. Here we report an alternative strategy utilized by an omnivorous marine worm, Hediste diversicolor, to supplement its diet: gardening by sprouting seeds. In addition to having many other known feeding modes, we showed using video recordings and manipulative mesocosm experiments that this species can also behave like gardeners by deliberately burying cordgrass seeds in their burrows, which has been previously shown to reduce the loss of seeds to water. These seeds, however, are protected by the seed husk, and we used feeding experiments to show that they were not edible for H. diversicolor until they had sprouted or the seed husk had been artificially removed. Additionally, sprouts were shown to be highly nutritious, permitting higher growth rates in H. diversicolor than the low-quality basal food, detritus. We propose both a proximate cause (seed husk as a physical barrier) and ultimate cause (nutritional demand) for this peculiar feeding behavior. Our findings suggest that sprouting may be a common strategy used by seed-collecting animals to exploit nutrients from well-protected seeds.

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.

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.

Habitat suitability modelling to improve understanding of seagrass loss and recovery and to guide decisions in relation to coastal discharge.

Habitat suitability modelling was used to test the relationship between coastal discharges and seagrass occurrence based on data from Adelaide (South Australia). Seven variables (benthic light including epiphyte shading, temperature, salinity, substrate, wave exposure, currents and tidal exposure) were simulated using a coupled hydrodynamic-biogeochemical model and interrogated against literature-derived thresholds for nine local seagrass species. Light availability was the most critical driver across the study area but wave exposure played a key role in shallow nearshore areas. Model validation against seagrass mapping data showed 86 % goodness-of-fit. Comparison against later mapping data suggested that modelling could predict ~745 ha of seagrass recovery in areas previously classified as 'false positives'. These results suggest that habitat suitability modelling is reliable to test scenarios and predict seagrass response to reduction of land-based loads, providing a useful tool to guide (investment) decisions to prevent loss and promote recovery of seagrasses.

Alternative mechanisms alter the emergent properties of self-organization in mussel beds.

Theoretical models predict that spatial self-organization can have important, unexpected implications by affecting the functioning of ecosystems in terms of resilience and productivity. Whether and how these emergent effects depend on specific formulations of the underlying mechanisms are questions that are often ignored. Here, we compare two alternative models of regular spatial pattern formation in mussel beds that have different mechanistic descriptions of the facilitative interactions between mussels. The first mechanism involves a reduced mussel loss rate at high density owing to mutual protection between the mussels, which is the basis of prior studies on the pattern formation in mussels. The second mechanism assumes, based on novel experimental evidence, that mussels feed more efficiently on top of mussel-generated hummocks. Model simulations point out that the second mechanism produces very similar types of spatial patterns in mussel beds. Yet the mechanisms predict a strikingly contrasting effect of these spatial patterns on ecosystem functioning, in terms of productivity and resilience. In the first model, where high mussel densities reduce mussel loss rates, patterns are predicted to strongly increase productivity and decrease the recovery time of the bed following a disturbance. When pattern formation is generated by increased feeding efficiency on hummocks, only minor emergent effects of pattern formation on ecosystem functioning are predicted. Our results provide a warning against predictions of the implications and emergent properties of spatial self-organization, when the mechanisms that underlie self-organization are incompletely understood and not based on the experimental study.