Seagrasses evolved from terrestrial plants into marine foundation species around 100 million years ago. Their ecological success, however, remains a mystery because natural organic matter accumulation within the beds should result in toxic sediment sulfide levels. Using a meta-analysis, a field study, and a laboratory experiment, we reveal how an ancient three-stage symbiosis between seagrass, lucinid bivalves, and their sulfide-oxidizing gill bacteria reduces sulfide stress for seagrasses. We found that the bivalve-sulfide-oxidizer symbiosis reduced sulfide levels and enhanced seagrass production as measured in biomass. In turn, the bivalves and their endosymbionts profit from organic matter accumulation and radial oxygen release from the seagrass roots. These findings elucidate the long-term success of seagrasses in warm waters and offer new prospects for seagrass ecosystem conservation.

In wetland soils and underwater sediments of marine, brackish and freshwater systems, the strong phytotoxin sulfide may accumulate as a result of microbial reduction of sulfate during anaerobiosis, its level depending on prevailing edaphic conditions. In this review, we compare an extensive body of literature on phytotoxic effects of this reduced sulfur compound in different ecosystem types, and review the effects of sulfide at multiple ecosystem levels: the ecophysiological functioning of individual plants, plant-microbe associations, and community effects including competition and facilitation interactions. Recent publications on multi-species interactions in the rhizosphere show even more complex mechanisms explaining sulfide resistance. It is concluded that sulfide is a potent phytotoxin, profoundly affecting plant fitness and ecosystem functioning in the full range of wetland types including coastal systems, and at several levels. Traditional toxicity testing including hydroponic approaches generally neglect rhizospheric effects, which makes it difficult to extrapolate results to real ecosystem processes. To explain the differential effects of sulfide at the different organizational levels, profound knowledge about the biogeochemical, plant physiological and ecological rhizosphere processes is vital. This information is even more important, as anthropogenic inputs of sulfur into freshwater ecosystems and organic loads into freshwater and marine systems are still much higher than natural levels, and are steeply increasing in Asia. In addition, higher temperatures as a result of global climate change may lead to higher sulfide production rates in shallow waters.

Summary 1.Populations of marine megaherbivores including green turtle (Chelonia mydas) have declined dramatically at a global scale as a result of overharvesting and habitat loss. This decline can be expected to also affect the tolerance of seagrass systems to coastal eutrophication. Until now, however, simultaneous effects of top-down control by megaherbivore grazing and bottom-up control by nutrient input have not been tested experimentally. 2. We therefore investigated the interacting effects of nutrient (N and P) addition and mimicked green turtle grazing on seagrass and epiphyte productivity, seagrass biomass and nutrient contents in exclosures at a pristine seagrass site in the Indo-Pacific region (Kalimantan, Indonesia). 3. Grazing almost doubled leaf biomass production rates, while nutrient addition (N+P, slowrelease granules) did not have an effect on these rates. Rhizome biomass was, however, strongly reduced by nutrient addition. In contrast to phosphorus, tissue nitrogen contents increased after nutrient addition, showing that nitrogen was not limiting primary productivity. Epiphyte growth was, however, strongly correlated with high water column P concentrations, indicating an indirect negative effect of eutrophication when turtle grazing would be absent. We calculated that green turtle leaf grazing leads to substantial exports of N and P, at rates of at least 8% of the standing stock per day equalling the daily seagrass production, up to 13 (N) and 1.4 (P) mg m )2 day )1 . 4. Synthesis. By combining our quantified effects with literature data, we propose a conceptual model of seagrass functioning under megaherbivore leaf grazing and eutrophication. In tropical seagrass systems with high green turtle grazing pressure, grazing alleviates the negative effects of eutrophication by the stimulation of seagrass production and concomitant nutrient uptake, the increased export of nutrients and the indirect prevention of low below-ground biomass. Similar to the role of terrestrial megaherbivores, these strong top-down controls show the pivotal role of green turtles in current coastal systems, which is lacking in systems where their numbers have greatly declined. These marine megaherbivores do not only drive structure and functioning of their foraging grounds but also increase the tolerance of seagrass ecosystems to eutrophication.

In many marine ecosystems, biodiversity critically depends on foundation species such as corals and seagrasses that engage in mutualistic interactions [1-3]. Concerns grow that environmental disruption of marine mutualisms exacerbates ecosystem degradation, with breakdown of the obligate coral mutualism ("coral bleaching") being an iconic example [2, 4, 5]. However, as these mutualisms are mostly facultative rather than obligate, it remains unclear whether mutualism breakdown is a common risk in marine ecosystems, and thus a potential accelerator of ecosystem degradation. Here, we provide evidence that drought triggered landscape-scale seagrass degradation and show the consequent failure of a facultative mutualistic feedback between seagrass and sulfide-consuming lucinid bivalves that in turn appeared to exacerbate the observed collapse. Local climate and remote sensing analyses revealed seagrass collapse after a summer with intense low-tide drought stress. Potential analysis-a novel approach to detect feedback-mediated state shifts-revealed two attractors (healthy and degraded states) during the collapse, suggesting that the drought disrupted internal feedbacks to cause abrupt, patch-wise degradation. Field measurements comparing degraded patches that were healthy before the collapse with patches that remained healthy demonstrated that bivalves declined dramatically in degrading patches with associated high sediment sulfide concentrations, confirming the breakdown of the mutualistic seagrass-lucinid feedback. Our findings indicate that drought triggered mutualism breakdown, resulting in toxic sulfide concentrations that aggravated seagrass degradation. We conclude that external disturbances can cause sudden breakdown of facultative marine mutualistic feedbacks. As this may amplify ecosystem degradation, we suggest including mutualisms in marine conservation and restoration approaches.

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.