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It is well known that seagrass meadows sequester atmospheric carbon dioxide, protect coasts, provide nurseries for global fisheries, and enhance biodiversity. Large-scale restoration of lost seagrass meadows is urgently needed to revive these planetary ecosystem services, but sourcing donor material from natural meadows would further decline them. Therefore, we advocate the domestication and mariculture of seagrasses in order to produce the large quantities of seed needed for successful rewilding of the sea with seagrass meadows. We provide a roadmap for our proposed solution and show that 44% of seagrass species have promising reproductive traits for domestication and rewilding by seeds. The principle of partially domesticating species to enable subsequent large-scale rewilding may form a successful shortcut to restore threatened keystone species and their vital ecosystem services.
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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.
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Ecossistema , Zosteraceae , Biomassa , PlantasRESUMO
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.
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Ecossistema , Recuperação e Remediação Ambiental , Phytophthora/patogenicidade , Zosteraceae/microbiologia , Conservação dos Recursos NaturaisRESUMO
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.
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Conservação dos Recursos Naturais , Ecossistema , Comportamento Alimentar , Tartarugas/fisiologia , Animais , Indonésia , Modelos Biológicos , Densidade DemográficaRESUMO
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.
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Poliquetos , Zosteraceae/crescimento & desenvolvimento , Animais , Biomassa , Ecossistema , Meio Ambiente , Sedimentos Geológicos , Folhas de Planta , Estações do Ano , Sulfetos/metabolismo , ÁguaRESUMO
Sargassum spp. strandings in the tropical Atlantic harm local ecosystems due to toxic sulfide levels. We conducted a mesocosm experiment to test the efficacy of iron(III) (hydr)oxides in (a) mitigating sulfide toxicity in mangroves resulting from Sargassum and (b) reducing potentially enhanced greenhouse gas emissions. Our results show that iron addition failed to prevent mangrove mortality caused by highly toxic sulfide concentrations, which reached up to 15,000 µmol l-1 in 14 days; timely removal may potentially prevent mangrove death. Sargassum-impacted mesocosms significantly increased methane, nitrous oxide, and carbon dioxide emissions, producing approximately 1 g CO2-equivalents m-2 h-1 during daylight hours, thereby shifting mangroves from sinks to sources of greenhouse gasses. However, iron addition decreased methane emissions by 62 % and nitrous oxide emissions by 57 %. This research reveals that Sargassum strandings have multiple adverse effects related to chemical and ecological dynamics in mangrove ecosystems, including greenhouse gas emissions.
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Metano , Óxido Nitroso , Sargassum , Sulfetos , Áreas Alagadas , Ferro , Poluentes Químicos da Água/toxicidade , Gases de Efeito Estufa/análiseRESUMO
Plant species usually have either annual or perennial life cycles, but facultative annual species have annual or perennial populations depending on their environment. In terrestrial angiosperms, facultative annual species are rare, with wild rice being one of the few examples. Our review shows that in marine angiosperms (seagrasses) facultative annual species are more common: six (of 63) seagrass species are facultative annual. It concerns Zostera marina, Z. japonica, Halophila decipiens, H. beccarii, Ruppia maritima, and R. spiralis. The annual populations generally produce five times more seeds than their conspecific perennial populations. Facultative annual seagrass species occur worldwide. Populations of seagrasses are commonly perennial, but the facultative annual species had annual populations when exposed to desiccation, anoxia-related factors, shading, or heat stress. A system-wide 'experiment' (closure of two out of three connected estuaries for large-scale coastal protection works) showed that the initial annual Z. marina population could shift to a perennial life cycle within 5 years, depending on environmental circumstances. We discuss potential mechanisms and implications for plant culture. Further exploration of flexible life histories in plant species, and seagrasses in particular, may aid in answering questions about trade-offs between vegetative and sexual reproduction, and preprogrammed senescence.
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In a seagrass restoration project, we explored the potential for enhancing the restoration process by excluding antagonistic engineering interactions (i.e., biomechanical warfare) between two ecosystem engineers: the bioturbating lugworm Arenicola marina and the sediment-stabilizing seagrass Zostera noltii Hornem. Applying a shell layer underneath half of our seagrass transplants successfully reduced adult lugworm density by over 80% and reduced lugworm-induced microtopography (a proxy for lugworm disturbance) at the wave-sheltered site. At the wave-exposed site adult lugworm densities and microtopography were already lower than at the sheltered site but were further reduced in the shell-treated units. Excluding lugworms and their bioengineering effects corresponded well with a strongly enhanced seagrass growth at the wave-sheltered site, which was absent at the exposed site. Enhanced seagrass growth in the present study was fully assigned to the removal of lugworms' negative engineering effects and not to any (indirect) evolving effects such as an altered biogeochemistry or sediment-stabilizing effects by the shell layer. The context-dependency implies that seagrass establishment at the exposed site is not constrained by negative ecosystem-engineering interactions only, but also by overriding physical stresses causing poor growth conditions. Present findings underline that, in addition to recent emphasis on considering positive (facilitating) interactions in ecological theory and practice, it is equally important to consider negative engineering interactions between ecosystem-engineering species. Removal of such negative interactions between ecosystem-engineering species can give a head start to the target species at the initial establishment phase, when positive engineering feedbacks by the target species on itself are still lacking. Though our study was carried out in a marine environment with variable levels of wave disturbance, similar principles may be expected to apply to other ecosystems that are inhabited by ecosystem engineers.
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Conservação dos Recursos Naturais/métodos , Ecossistema , Monitoramento Ambiental/métodos , Poliquetos/fisiologia , Zosteraceae/fisiologia , Animais , Sedimentos Geológicos , Herbivoria , Oceanos e MaresRESUMO
The spatial structure of seagrass landscapes is typically ascribed to the direct influence of physical factors such as hydrodynamics, light, and sediment transport. We studied regularly interspaced banded patterns, formed by elongated patches of seagrass, in a small-scale intertidal ecosystem. We investigated (1) whether the observed spatial patterns may arise from feedback interactions between seagrass and its abiotic environment and (2) whether changes in abiotic conditions may lead to predictable changes in these spatial patterns. Field measurements, experiments, and a spatially explicit computer model identified a "scale-dependent feedback" (a mechanism for spatial self-organization) as a possible cause for the banded patterns. Increased protection from uprooting by improved anchoring with increasing seagrass density caused a local positive feedback. Sediment erosion around seagrass shoots increased with distance through the seagrass bands, hence causing a long-range negative feedback. Measurements across the depth gradient of the intertidal, together with model simulations, demonstrated that seagrass cover and mean patch size were predictably influenced by additional external stress caused by light limitation and desiccation. Thus, our study provides direct empirical evidence for a consistent response of spatial self-organized patterns to changing abiotic conditions, suggesting a potential use for self-organized spatial patterns as stress indicators in ecosystems.
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Demografia , Ecossistema , Magnoliopsida , Modelos Biológicos , Oceanos e Mares , Brotos de PlantaRESUMO
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.
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Adaptação Fisiológica , Recuperação e Remediação Ambiental/métodos , Hydrocharitaceae/fisiologia , Áreas Alagadas , Zosteraceae/fisiologia , Plásticos Biodegradáveis , Biomimética/métodos , Ecologia/métodos , Recuperação e Remediação Ambiental/instrumentação , Florida , Países Baixos , Água do Mar , Suécia , Clima Tropical , Índias OcidentaisRESUMO
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.
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Seagrass meadows, key ecosystems supporting fisheries, carbon sequestration and coastal protection, are globally threatened. In Europe, loss and recovery of seagrasses are reported, but the changes in extent and density at the continental scale remain unclear. Here we collate assessments of changes from 1869 to 2016 and show that 1/3 of European seagrass area was lost due to disease, deteriorated water quality, and coastal development, with losses peaking in the 1970s and 1980s. Since then, loss rates slowed down for most of the species and fast-growing species recovered in some locations, making the net rate of change in seagrass area experience a reversal in the 2000s, while density metrics improved or remained stable in most sites. Our results demonstrate that decline is not the generalised state among seagrasses nowadays in Europe, in contrast with global assessments, and that deceleration and reversal of declining trends is possible, expectingly bringing back the services they provide.
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Magnoliopsida/crescimento & desenvolvimento , Biodiversidade , Conservação dos Recursos Naturais , Ecossistema , Europa (Continente) , História do Século XX , História do Século XXI , Magnoliopsida/classificação , Biologia Marinha/históriaRESUMO
We examined the original manuscripts of a French national survey conducted in 1933 on the state of common eelgrass Zostera marina beds along the French Atlantic coasts during the period when wasting disease struck the entire North Atlantic population in the 1930s. Based on GIS related techniques and old sets of aerial photographs, we present the first accurate mapping of the Z. marina beds before wasting disease occurred and assess their spatial recolonization since the 1950s in the Chausey Archipelago (France), which contains large Z. marina beds. The national survey confirmed that the Z. marina beds almost totally disappeared from the French coasts during the 1930s. However, the disease symptoms seem to have begun locally a few years before. On the study site, we found that the Z. marina beds were more than twice as extended than as they are today, and covered both subtidal and intertidal areas. By the 1950s, 20 yr after the onset of the disease, the beds had hardly recolonized, and contrary to the recolonization patterns reported elsewhere in Europe, they were mainly restricted to subtidal areas. The subtidal and intertidal Z. marina beds on the site are now rapidly expanding.
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Doenças das Plantas , Zosteraceae , Oceano Atlântico , França , Sistemas de Informação GeográficaRESUMO
The limiting effects of stressors like desiccation, light and salinity on seagrass growth and distribution are well-studied. However, little is known about their interactive effects, and whether such effects might differ among populations that are adapted to different local conditions. In two laboratory experiments we tested (a) if growth and development of intertidal, temperate Zostera noltii is affected by emergence time (experiment 1 and 2), and (b) how this is affected by an additional, second stressor, namely shading (experiment 1) or high salinity (25, 30 and 35, experiment 2). In addition, we tested (c) whether the effects of emergence time and salinity varied between three different European seagrass populations (Saint-Jacut/France, Oosterschelde/The Netherlands, and Sylt/Germany), which are likely adapted to different salinity levels (experiment 2). In both experiments, emergence of 8 h per tidal cycle (of 12 h) had a negative effect on seagrass relative growth rate (RGR), and aboveground biomass. Emergence furthermore reduced either rhizome length (experiment 1) or belowground biomass (experiment 2). Shading (experiment 1) resulted in lower RGR and a two-fold higher aboveground/belowground ratio. We found no interactive effects of emergence and shading stress. Salinity (experiment 2) did not affect seagrass growth or morphology of any of the three populations. The three tested populations differed greatly in morphology but showed no differential response to emergence or salinity level (experiment 2). Our results indicate that emergence time and shading show an additive negative effect (no synergistic or antagonistic effect), making the plants still vulnerable to such combination, a combination that may occur as a consequence of self-shading during emergence or resulting from algal cover. Emergence time likely determines the upper limit of Z. noltii and such shading will likely lower the upper limit. Shading resulted in higher aboveground/belowground ratios as is a general response in seagrass. Z. noltii of different populations originating from salinity 30 and 35 seem tolerant to variations in salinity within the tested range. Our results indicate that the three tested populations show morphotypic rather than ecotypic variation, at least regarding the salinity and emergence, as there were no interactive effects with origin. For restoration, this implies that the salinity regime of the donor and receptor site of Z. noltii is of no concern within the salinity range 25-35.
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Seagrass meadows form highly productive and valuable ecosystems in the marine environment. Throughout the year, seagrass meadows are exposed to abiotic and biotic variations linked to (i) seasonal fluctuations, (ii) short-term stress events such as, e.g., local nutrient enrichment, and (iii) small-scale disturbances such as, e.g., biomass removal by grazing. We hypothesized that short-term stress events and small-scale disturbances may affect seagrass chance for survival in temperate latitudes. To test this hypothesis we focused on seagrass carbon reserves in the form of starch stored seasonally in rhizomes, as these have been defined as a good indicator for winter survival. Twelve Zostera noltei meadows were monitored along a latitudinal gradient in Western Europe to firstly assess the seasonal change of their rhizomal starch content. Secondly, we tested the effects of nutrient enrichment and/or biomass removal on the corresponding starch content by using a short-term manipulative field experiment at a single latitude in the Netherlands. At the end of the growing season, we observed a weak but significant linear increase of starch content along the latitudinal gradient from south to north. This agrees with the contention that such reserves are essential for regrowth after winter, which is more severe in the north. In addition, we also observed a weak but significant positive relationship between starch content at the beginning of the growing season and past winter temperatures. This implies a lower regrowth potential after severe winters, due to diminished starch content at the beginning of the growing season. Short-term stress and disturbances may intensify these patterns, because our manipulative experiments show that when nutrient enrichment and biomass loss co-occurred at the end of the growing season, Z. noltei starch content declined. In temperate zones, the capacity of seagrasses to accumulate carbon reserves is expected to determine carbon-based regrowth after winter. Therefore, processes affecting those reserves might affect seagrass resilience. With increasing human pressure on coastal systems, short- and small-scale stress events are expected to become more frequent, threatening the resilience of seagrass ecosystems, particularly at higher latitudes, where populations tend to have an annual cycle highly dependent on their storage capacity.
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A manipulative field experiment was designed to investigate the effects of sediment-nutrients and sediment-organic matters on seagrasses, Zostera japonica, using individual and population indicators. The results showed that seagrasses quickly responded to sediment-nutrient and organic matter loading. That is, sediment-nutrients positively impacted on seagrasses by increasing N content of leaves and roots, leaf length and belowground biomass. Sediment-organic matter loading lowered N content of seagrass leaves and belowground biomass. Negative effects of organic matter loading were aggravated during nutrient loading, by decreasing N content of leaves, P content of roots, leaf width, shoot number in the middle period of the experiment, increasing C/N ratio of leaves, C/P and N/P ratio of roots and above to belowground biomass ratio of seagrasses. Consequently, Z. japonica could be considered as a fast indicator to monitor seagrass ecosystem status in the eutrophic areas and facilitate to interpreting the response of seagrasses to multiple stressors.
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Monitoramento Ambiental , Poluentes da Água/análise , Zosteraceae/fisiologia , Biomassa , Ecossistema , Nitrogênio/análise , Fósforo/análise , Folhas de Planta/fisiologiaRESUMO
Seagrass meadows are vital ecosystems in coastal zones worldwide, but are also under global threat. One of the major hurdles restricting the success of seagrass conservation and restoration is our limited understanding of ecological feedback mechanisms. In these ecosystems, multiple, self-reinforcing feedbacks can undermine conservation efforts by masking environmental impacts until the decline is precipitous, or alternatively they can inhibit seagrass recovery in spite of restoration efforts. However, no clear framework yet exists for identifying or dealing with feedbacks to improve the management of seagrass ecosystems. Here we review the causes and consequences of multiple feedbacks between seagrass and biotic and/or abiotic processes. We demonstrate how feedbacks have the potential to impose or reinforce regimes of either seagrass dominance or unvegetated substrate, and how the strength and importance of these feedbacks vary across environmental gradients. Although a myriad of feedbacks have now been identified, the co-occurrence and likely interaction among feedbacks has largely been overlooked to date due to difficulties in analysis and detection. Here we take a fundamental step forward by modelling the interactions among two distinct above- and belowground feedbacks to demonstrate that interacting feedbacks are likely to be important for ecosystem resilience. On this basis, we propose a five-step adaptive management plan to address feedback dynamics for effective conservation and restoration strategies. The management plan provides guidance to aid in the identification and prioritisation of likely feedbacks in different seagrass ecosystems.
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Alismatales/fisiologia , Conservação dos Recursos Naturais , Ecossistema , Ecologia , Meio AmbienteRESUMO
Excess nutrients are potential factors that drive phase shifts from seagrasses to macroalgae. We carried out a manipulative field experiment to study the effects of macroalgae Ulva pertusa loading and nutrient addition to the water column on the nitrogen (N) and carbon (C) contents (i.e., fast indicators) as well as on the morphology and structure (i.e., slow indicators) of Zostera marina. Our results showed rapid impact of increased macroalgae and nutrient load on Z. marina C/N ratios. Also, macroalgae addition resulted in a trend of decreasing belowground biomass of seagrasses, and nutrient load significantly decreased above to belowground biomass ratio. Although some morphological/structural variables showed relatively fast responses, the effects of short-term disturbance by macroalgae and nutrients were less often significant than on physiological variables. Monitoring of seagrass physiological indicators may allow for early detection of eutrophication, which may initiate timely management interventions to avert seagrass loss.
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Monitoramento Ambiental , Eutrofização , Alga Marinha/crescimento & desenvolvimento , Zosteraceae/fisiologia , Biomassa , Nitrogênio/análise , Fósforo/análise , Ulva , Poluentes da Água/análiseRESUMO
Despite being a highly valuable key-stone ecosystem, seagrass meadows are threatened and declining worldwide, creating urgent need for indicators of their health status. We compared two indicators for seagrass health: standing leaf area index versus relative recovery from local disturbance. Disturbance was created by removing aboveground biomass and recording the rate of regrowth for Zostera marina meadows exposed to contrasting wave regimes and nutrient stress levels. Within the experimental period, relative regrowth in gaps was around 50% in most plots, except for the ambient nutrient treatment at the sheltered site, where it exceeded 100%. The two indicators showed an opposite response to disturbance: the higher the standing leaf area index, the lower the relative recovery from disturbance. This conflicting response raises the question on the proper interpretation of such indicators to estimate seagrass health and resilience, and how to ideally monitor seagrass ecosystems in order to predict collapse.