Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore.

Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.

Seed settling and trapping during submerged secondary dispersal: Implications for saltmarsh recruitment and restoration.

Given the decline of global salt marshes, there is a pressing need to pinpoint the key processes that limit and facilitate seed-based pioneer recruitment. Secondary seed dispersal, in the form of short-distance submerged movement, is a prerequisite for initiating pioneer establishment in adjacent tidal flats but has not been fully appreciated and understood. In this study, using a settling tube and race-track flume, seeds of four global occurring saltmarsh species were studied in terms of their settlement speed and trapping opportunity to understand how seed traits and physical settings affect submerged dispersal behavior and thus seed-based saltmarsh recruitment. Present study led to the following novel insights: 1) Seeds have density-dependent settling speeds, which are comparable to that of fine sand, but much faster than that of very fine sand and silt. Since the latter is the type of sediment commonly found in many estuaries worldwide (such as the Scheldt), seeds will typically settle faster than local sediments. A sufficiently long hydrodynamic-calm period allows slowly settling sediment to bury settled seeds, otherwise, seeds will remain uncovered if the period is short. 2) Seed trapping ratio increased linearly with surface roughness (a proxy for local topographic complexity), but this effect becomes smaller with increasing hydrodynamic intensity. Seed drag coefficient was identified as the key biotic factor contributing to interspecies variability in trapping ratio. Overall, present results suggest that submerged seed dispersal may form a primary bottleneck for salt marsh recruitment by limiting seed availability via two mechanisms: i) reduced chance of seed burial through asynchronous settling of seeds and sediment particles; ii) reduced probability of seed trapping due to encountering smooth tidal flat surfaces. This study provide mechanistic and data basis for the targeted application of biophysical models in predicting outcomes of saltmarsh recruitment and long-term maintenance, thereby informing seed-based conservation and restoration.

The importance of marshes providing soil stabilization to resist fast-flow erosion in case of a dike breach.

Salt marshes provide valuable ecosystem services including coastal protection by reducing wave loading on dikes and seawalls. If the topsoil is erosion resistant to fast-flowing water, it may also reduce breach depth if a dike fails. In this experiment, we quantified the topsoil erosion resistance from marshes and bare tidal flats with different soil types to understand the extent to which they can help reduce breach depth. Intact soil samples were collected from 11 locations in the Netherlands at different tidal elevations and then exposed for 3 h to 2.3 m/s currents. To the samples that remained stable after flow exposure, an artificial crack was made to test their stability following soil disturbance. All samples from the tidal flats were completely eroded, regardless of sediment type. In contrast, all samples from well-established marsh plateaus were stable as long as no disturbances were made, including those with sandy subsoils. After creating artificial cracks, samples with a thin cohesive top layer on top of sandy subsoil collapsed, while marshes with silty subsoils remained stable. Pioneer marshes on sandy substrate without a cohesive top layer were the only vegetated soils that completely eroded. The lower erosion of marshes with either sandy or silty soils compared to bare tidal flats was best explained by the presence of a top layer with belowground biomass, high organic content, high water content, and low bulk density. When analyzing the erodibility of marshes only, fine root density was the best predictor of erosion resistance. This study demonstrates the importance of preserving, restoring, or creating salt marshes, to obtain a topsoil that is erosion resistant under fast-flowing water, which helps reduce breach dimensions if a dike fails. The probability of topsoil erosion in established marshes with sandy subsoil is higher than in silty marshes. A silty layer of cohesive sediment on top of the sand provides extra erosion resistance as long as it does not break. Pioneer marshes that have not developed a cohesive top layer are erosion sensitive, especially in sandy soils. For future marsh creations, using fine-grained sediments or a mixture of sand with silt or clay is recommended.

Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversity.

Habitat-forming species sustain biodiversity and ecosystem functioning in harsh environments through the amelioration of physical stress. Nonetheless, their role in shaping patterns of species distribution under future climate scenarios is generally overlooked. Focusing on coastal systems, we assess how habitat-forming species can influence the ability of stress-sensitive species to exhibit plastic responses, adapt to novel environmental conditions, or track suitable climates. Here, we argue that habitat-former populations could be managed as a nature-based solution against climate-driven loss of biodiversity. Drawing from different ecological and biological disciplines, we identify a series of actions to sustain the resilience of marine habitat-forming species to climate change, as well as their effectiveness and reliability in rescuing stress-sensitive species from increasingly adverse environmental conditions.

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.

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.

The role of seasonality in reproduction of multiannual delayed gametophytes of Saccharina latissima.

Delayed gametophytes are able to grow vegetatively for prolonged periods of time. As such, they are potentially very valuable for kelp aquaculture given their great promise in opening up novel opportunities for kelp breeding and farming. However, large-scale application would require more in-depth understanding of how to control reproduction in delayed gametophytes. For newly formed gametophytes, many environmental factors for reproduction have been identified, with key drivers being light intensity, temperature, and the initial gametophyte density. However, the question of whether delayed gametophytes react similarly to these life cycle controls remains open for exploration. In this study, we performed a full factorial experiment on the influences of light intensity, temperature, and density on the reproduction of multiannual delayed gametophytes of Saccharina latissima, during which the number of sporophytes formed was counted. We demonstrate that delayed gametophytes of S. latissima can reliably reproduce sexually after more than a year of vegetative growth, depending on the effects between light intensity and temperature. Under higher light intensities (≥29 µmol photons · m-2 · s-1 ), optimal reproduction was observed at lower temperatures (10.2°C), while at lower light intensities (≤15 µmol photons · m-2 · s-1 ), optimal reproduction was observed at higher temperatures (≥12.6°C). Given the seasonal lag between solar radiation and sea surface temperature in natural systems, these conditions resemble those found during spring (i.e., increasing light intensity with low temperatures) and autumn (i.e., decreasing light intensity with higher temperatures). Seasonality can be used as an aquaculture tool to better control the reproduction of delayed gametophytes.

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.

Biomechanical properties of marsh vegetation in space and time: effects of salinity, inundation and seasonality.

BACKGROUND AND AIMS: Over the last decade, the importance of plant biomechanical properties in shaping wave dissipation efficiency of marsh vegetation has gained growing attention. Here we provide the first analyses of how biomechanical stem properties vary with seasons and along environmental gradients in coastal and estuarine marshes, which is essential to enable accurate assessments of flood defence value of marsh vegetation. METHODS: We quantified both spatial and seasonal variation in stem flexibility and breakability for a variety of common marsh vegetation (Spartina anglica, Scirpus maritimus, Phragmites australis, Elymus athericus, Suaeda maritima, Aster tripolium, Saliconia procumbens) distributed along both salinity and inundation gradients. KEY RESULTS: Increasing salinity tends to induce a shift from species with tall shoots, high flexural stiffness (stem resistance to bending; N mm2) towards species with shorter and more flexible stems. The same trend was found with increasing inundation stress (i.e. decreasing elevation) from the higher part of the low marsh towards the pioneer zone. Stem breakability (the force required to break or fold a stem, N) followed the same pattern of stem stiffness due to the positive relationship between flexural strength (material resistance to flexure, N mm-2) and Young's bending modulus (material resistance to bending; N mm-2). Shifts in stem stiffness and breakability at the community level were found to relate positively to the variation in canopy height between species, highlighting the concurrence of changes in morphological and biomechanical traits under environmental changes. Compared to the differences between species, within-species variability between sampling locations and between seasons is generally minor. CONCLUSIONS: Our findings imply that environmental changes may significantly modify wave attenuation capacity of coastal vegetation by inducing species shifts. This emphasizes the need to understand the response of community composition to climate change and human disturbances, when using nature-based flood protection by coastal vegetation as an adaptive response to global change.

The gathering storm: optimizing management of coastal ecosystems in the face of a climate-driven threat.

BACKGROUND: The combination of rising sea levels and increased likelihood of extreme storm events poses a major threat to our coastlines and as a result, many ecosystems recognized and valued for their important contribution to coastal defence face increased damage from erosion and flooding. Nevertheless, only recently have we begun to examine how plant species and communities, respond to, and recover from, the many disturbances associated with storm events. SCOPE: We review how the threats posed by a combination of sea level rise and storms affects coastal sub-, inter- and supra-tidal plant communities. We consider ecophysiological impacts at the level of the individual plant, but also how ecological interactions at the community level, and responses at landscape scale, inform our understanding of how and why an increasing frequency and intensity of storm damage are vital to effective coastal management. While noting how research is centred on the impact of hurricanes in the US Gulf region, we take a global perspective and consider how ecosystems worldwide (e.g. seagrass, kelp forests, sand dunes, saltmarsh and mangroves) respond to storm damage and contribute to coastal defence. CONCLUSIONS: The threats posed by storms to coastal plant communities are undoubtedly severe, but, beyond this obvious conclusion, we highlight four research priority areas. These call for studies focusing on (1) how storm disturbance affects plant reproduction and recruitment; (2) plant response to the multiple stressors associated with anthropogenic climate change and storm events; (3) the role of ecosystem-level interactions in dictating post-disturbance recovery; and (4) models and long-term monitoring to better predict where and how storms and other climate change-driven phenomena impact coastal ecosystems and services. In so doing, we argue how plant scientists must work with geomorphologists and environmental agencies to protect the unique biodiversity and pivotal contribution to coastal defence delivered by maritime plant communities.

Physiological and biochemical responses of the salt-marsh plant Spartina alterniflora to long-term wave exposure.

BACKGROUND AND AIMS: Ecosystem-based flood defence including salt-marsh as a key component is increasingly applied worldwide due to its multifunctionality and cost-effectiveness. While numerous experiments have explored the wave-attenuation effects of salt-marsh plants critical to flood protection, little is known about the physiological and biochemical responses of these species to continuous wave exposure. METHODS: To address this knowledge gap, we developed a shallow-water wave simulator to expose individual Spartina alterniflora plants to waves in a greenhouse for 8 weeks. S. alterniflora individuals were partially submerged and experienced horizontal sinusoidal motion to mimic plant exposure to shallow water waves. A factorial experiment was used to test the effects of three wave heights (4.1 cm, 5.5 cm and a no-wave control) and two wave periods (2 s and 3 s) on the following key physiological and biochemical plant parameters: plant growth, antioxidant defence and photosynthetic capacity. KEY RESULTS: Comparison of wave treatment and control groups supported our hypotheses that wave exposure leads to oxidative stress in plants and suppresses plant photosynthetic capacity and thereby growth. In response, the wave-exposed plants exhibited activated antioxidant enzymes. Comparison between the different wave treatment groups suggested the wave effects to be generally correlated positively with wave height and negatively with wave period, i.e. waves with greater height and frequency imposed more stress on plants. In addition, wave-exposed plants tended to allocate more biomass to their roots. Such allocation is favourable because it enhances root anchorage against the wave impact. CONCLUSIONS: Simulated wave exposure systems such as the one used here are an effective tool for studying the response of salt-marsh plants to long-term wave exposure, and so help inform ecosystem-based flood defence projects in terms of plant selection, suitable transplantation locations and timing, etc. Given the projected variability of the global wave environment due to climate change, understanding plant response to long-term wave exposure has important implications for salt-marsh conservation and its central role in natural flood defence.

Elevated micro-topography boosts growth rates in Salicornia procumbens by amplifying a tidally driven oxygen pump: implications for natural recruitment and restoration.

BACKGROUND AND AIMS: The growth rate of pioneer species is known to be a critical component determining recruitment success of marsh seedlings on tidal flats. By accelerating growth, recruits can reach a larger size at an earlier date, which reduces the length of the disturbance-free window required for successful establishment. Therefore, the pursuit of natural mechanisms that accelerate growth rates at a local scale may lead to a better understanding of the circumstances under which new establishment occurs, and may suggest new insights with which to perform restoration. This study explores how and why changes in local sediment elevation modify the growth rate of recruiting salt marsh pioneers. METHODS: A mesocosm experiment was designed in which the annual salt marsh pioneer Salicornia procumbens was grown over a series of raised, flat and lowered sediment surfaces, under a variety of tidal inundation regimes and in vertically draining or un-draining sediment. Additional physical tests quantified the effects of these treatments on sediment water-logging and oxygen dynamics, including the use of a planar optode experiment. KEY RESULTS: In this study, the elevation of sediment micro-topography by 2 cm was the overwhelming driver of plant growth rates. Seedlings grew on average 25 % faster on raised surfaces, which represented a significant increase when compared to other groups. Changes in growth aligned well with the amplifying effect of raised sediment beds on a tidally episodic oxygenation process wherein sediment pore spaces were refreshed by oxygen-rich water at the onset of high tide. CONCLUSIONS: Overall, the present study suggests this tidally driven oxygen pump as an explanation for commonly observed natural patterns in salt marsh recruitment near drainage channels and atop raised sediment mounds and reveals a promising way forward to promote the establishment of pioneers in the field.

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.

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.

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.

Marine Phytophthora species can hamper conservation and restoration of vegetated coastal ecosystems.

Phytophthora species are potent pathogens that can devastate terrestrial plants, causing billions of dollars of damage yearly to agricultural crops and harming fragile ecosystems worldwide. Yet, virtually nothing is known about the distribution and pathogenicity of their marine relatives. This is surprising, as marine plants form vital habitats in coastal zones worldwide (i.e. mangrove forests, salt marshes, seagrass beds), and disease may be an important bottleneck for the conservation and restoration of these rapidly declining ecosystems. We are the first to report on widespread infection of Phytophthora and Halophytophthora species on a common seagrass species, Zostera marina (eelgrass), across the northern Atlantic and Mediterranean. In addition, we tested the effects of Halophytophthora sp. Zostera and Phytophthora gemini on Z. marina seed germination in a full-factorial laboratory experiment under various environmental conditions. Results suggest that Phytophthora species are widespread as we found these oomycetes in eelgrass beds in six countries across the North Atlantic and Mediterranean. Infection by Halophytophthora sp. Zostera, P. gemini, or both, strongly affected sexual reproduction by reducing seed germination sixfold. Our findings have important implications for seagrass ecology, because these putative pathogens probably negatively affect ecosystem functioning, as well as current restoration and conservation efforts.

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.

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.

Seagrasses are negatively affected by organic matter loading and Arenicola marina activity in a laboratory experiment.

When two ecosystem engineers share the same natural environment, the outcome of their interaction will be unclear if they have contrasting habitat-modifying effects (e.g., sediment stabilization vs. sediment destabilization). The outcome of the interaction may depend on local environmental conditions such as season or sediment type, which may affect the extent and type of habitat modification by the ecosystem engineers involved. We mechanistically studied the interaction between the sediment-stabilizing seagrass Zostera noltii and the bioturbating and sediment-destabilizing lugworm Arenicola marina, which sometimes co-occur for prolonged periods. We investigated (1) if the negative sediment destabilization effect of A. marina on Z. noltii might be counteracted by positive biogeochemical effects of bioirrigation (burrow flushing) by A. marina in sulfide-rich sediments, and (2) if previously observed nutrient release by A. marina bioirrigation could affect seagrasses. We tested the individual and combined effects of A. marina presence and high porewater sulfide concentrations (induced by organic matter addition) on seagrass biomass in a full factorial lab experiment. Contrary to our expectations, we did not find an effect of A. marina on porewater sulfide concentrations. A. marina activities affected the seagrass physically as well as by pumping nutrients, mainly ammonium and phosphate, from the porewater to the surface water, which promoted epiphyte growth on seagrass leaves in our experimental set-up. We conclude that A. marina bioirrigation did not alleviate sulfide stress to seagrasses. Instead, we found synergistic negative effects of the presence of A. marina and high sediment sulfide levels on seagrass biomass.