Patch age alters seagrass response mechanisms to herbivory damage.

Natural disturbances can produce a mosaic of seagrass patches of different ages, which may affect the response to herbivory. These pressures can have consequences for plant performance. To assess how seagrass patch age affects the response to herbivory, we simulated the effect of herbivory by clipping leaves of Halodule wrightii in patches of 2, 4 and 6 years. All clipped plants showed ability to compensate herbivory by increasing leaf growth rate (on average 4.5-fold). The oldest patches showed resistance response by increasing phenolic compounds (1.2-fold). Contrastingly, the concentration of phenolics decreased in the youngest patches (0.26-fold), although they had a similar leaf carbon content to controls. These results suggest that younger plants facing herbivory pressure reallocate their phenolic compounds towards primary metabolism. Results confirm the H. wrightii tolerance to herbivory damage and provides evidence of age-dependent compensatory responses, which may have consequences for seagrass colonization and growth in perturbed habitats.

Rosmarinic Acid and Flavonoids of the Seagrass Zostera noltei: New Aspects on Their Quantification and Their Correlation with Sunlight Exposure.

Seagrasses are plants adapted to the marine environment that inhabit shallow coastal waters, where they may be exposed to direct sunlight during low tides. These plants have photoprotection mechanisms, which could include the use of phenolic secondary metabolites. In this study, rosmarinic acid (RA) and the flavonoids of Zostera noltei from the Bay of Cadiz (Spain) have been analyzed, first to define suitable conditions of leaves (i.e., fresh, dried, or frozen) for quantitative analysis, and then to explore the potential correlation between the phenolic profile of the leaves and sunlight exposure using an in situ experimental approach. Compared with fresh leaves, the contents of RA and flavonoids were significantly lower in air-dried and freeze-dried leaves. Freezing caused highly variable effects on RA and did not affect to flavonoid levels. On the other hand, the content of RA was significantly higher in plants that emerged during low tides than in plants permanently submerged, while plants underneath an artificial UV filter experienced a progressive reduction in RA content. However, the major flavonoids did not show a clear response to sunlight exposure and were unresponsive to diminished UV incidence. The results showed a positive correlation of RA with direct sunlight and UV exposure of leaves, suggesting that this compound contributes to the photoprotection of Z. noltei.

Comparison of macroplastics dynamic across a tidal-dominated coastal habitat seascape including seagrasses, salt marshes, rocky bottoms and soft sediments.

Coastal environments are usually composed by heterogeneous coastal-seascape, which can modify macroplastics accumulation dynamic. We evaluated seasonally the litter trapped on tidal-dominated habitats including two seagrass species, salt marsh, sandy beach, bare sediment and rocky bottom. Vegetated habitats showed the highest plastic accumulation in autumn-winter seasons, especially in medium-lower tidal-elevation zones. Seagrasses accumulated most of the degraded macroplastics, whereas averaged smaller sizes of litter were found in the salt marsh. The trapping ability of macrophytes was related to aboveground-biomass properties (i.e., height, width or flexibility) rather than shoot-density. Sandy beaches exhibited the highest plastics accumulation matching with the touristic-peak in the area, whereas rocky bottom was an important sink for macroplastics. This study provides authorities with comprehensible information to address the marine plastic litter problem taking into account the habitat-connectivity, the litter trap-ability of macrophytes and the tidal-elevation influence in order to improve future actions to deal with plastic pollution.

Changes in carbon metabolism and dissolved organic carbon fluxes on seagrass patches (Halodule wrightii) with different ages in Southern Gulf of California.

Seagrass meadows are highly dynamic, particularly in sites where extreme climatological events may produce a mosaic of patches with different ages. This study evaluates the community carbon metabolism, dissolved organic carbon (DOC) fluxes and associated fauna in patches of Halodule wrightii with different ages since establishment. Net community production declined as patch age increased, probably due to the increase in non-photosynthetic tissues, higher respiration rates of the community assemblage and a likely increase in self-shading of the canopy. The export of DOC was significantly higher in the youngest patches, mainly as a consequence of the lower seagrass net production recorded in older meadows. We concluded that 'colonizers' seagrass species may show higher production rates and DOC release during the first stages of colonization, which suggest that, the production, organic carbon exportation and their role as relevant blue carbon communities may be higher than expected.

Resistance and recovery of benthic marine macrophyte communities to light reduction: Insights from carbon metabolism and dissolved organic carbon (DOC) fluxes, and implications for resilience.

A crucial factor in the long-term survival of benthic macrophyte communities under light-reduction stress is how they balance carbon metabolism during photosynthesis and respiration. In turn, the dissolved organic carbon (DOC) released by these communities, which can be highly light-dependent, stands as a source of carbon, fuelling marine communities and playing an important role in the ocean carbon sequestration. This is the first study to evaluate light-reduction stress and recovery in the seagrass Zostera noltei and the macroalga Caulerpa prolifera. Light reduction led to a significant decrease in the production of both communities from autotrophic to heterotrophic. Results indicated that most of the DOC released by vegetated coastal communities comes from photosynthetic activity, and that the net DOC fluxes can be greatly affected by shading events. Finally, both communities showed resilience underpinned by high recovery but low resistance capacity, with C. prolifera showing the highest resilience to unfavourable light conditions.

Sedimentary organic carbon and nitrogen stocks of intertidal seagrass meadows in a dynamic and impacted wetland: Effects of coastal infrastructure constructions and meadow establishment time.

Seagrass meadows, through their large capacity to sequester and store organic carbon in their sediments, contribute to mitigate climatic change. However, these ecosystems have experienced large losses and degradation worldwide due to anthropogenic and natural impacts and they are among the most threatened ecosystems on Earth. When a meadow is impacted, the vegetation is partial- or completely lost, and the sediment is exposed to the atmosphere or water column, resulting in the erosion and remineralisation of the carbon stored. This paper addresses the effects of the construction of coastal infrastructures on sediment properties, organic carbon, and total nitrogen stocks of intertidal seagrass meadows, as well as the size of such stocks in relation to meadow establishing time (recently and old established meadows). Three intertidal seagrass meadows impacted by coastal constructions (with 0% seagrass cover at present) and three adjacent non-impacted old-established meadows (with 100% seagrass cover at present) were studied along with an area of bare sediment and two recent-established seagrass meadows. We observed that the non-impacted areas presented 3-fold higher percentage of mud and 1.5 times higher sedimentary organic carbon stock than impacted areas. Although the impacted area was relatively small (0.05-0.07 ha), coastal infrastructures caused a significant reduction of the sedimentary carbon stock, between 1.1 and 2.2 Mg OC, and a total loss of the carbon sequestration capacity of the impacted meadow. We also found that the organic carbon stock and total nitrogen stock of the recent-established meadow were 30% lower than those of the old-established ones, indicating that OC and TN accumulation within the meadows is a continuous process, which has important consequences for conservation and restoration actions. These results contribute to understanding the spatial variability of blue carbon and nitrogen stocks in coastal systems highly impacted by urban development.

Differential effects of nutrient enrichment on carbon metabolism and dissolved organic carbon (DOC) fluxes in macrophytic benthic communities.

Nutrient enrichment can alter negatively benthic communities and reduce their ecological services. This study explores in two contrasting seasons (winter and summer), the effects of in situ nutrient enrichment at the community level on carbon metabolism and dissolved organic carbon (DOC) fluxes in two benthic communities dominated by the seagrass Cymodocea nodosa and by the macroalga Caulerpa prolifera. Under nutrient enrichment, C. nodosa increased total community biomass and diversity in summer, while net community production shifted from net autotrophic to net heterotrophic in winter. In contrast, C. prolifera became heterotrophic in summer, while no significant effects were found in winter. Regarding DOC fluxes, nutrient enrichment shifted C. nodosa from net DOC consumer in winter to a strong net DOC producer in summer, while C. prolifera seemed unaffected. Therefore, nutrient enrichment can promote conditional effects (positive, negative or neutral) in coastal areas depending both on macrophyte assemblages and season.

Effect of In Situ short-term temperature increase on carbon metabolism and dissolved organic carbon (DOC) fluxes in a community dominated by the seagrass Cymodocea nodosa.

Seagrasses form one of the most productive and threatened ecosystems worldwide because of global change and anthropogenic pressures. The frequency of extreme climatic events, such as heat waves, are expected to increase and may drive even more adverse effects than gradual warming. This study explores for the first time the effects of a sudden and temporary increase of temperature in situ on carbon metabolism and dissolved organic carbon (DOC) fluxes in a community dominated by a seagrass (Cymodocea nodosa) during two contrasting seasons (winter and summer). Results showed a positive correlation between temperature and seagrass production between seasons, while the experimental sudden and temporary increase in water temperature did not produce significant differences in carbon community metabolism and DOC fluxes in winter. In contrast, high temperature conditions in summer enhanced significantly the net community production and affected positively to DOC fluxes. Hence, this study indicates that a sudden and temporary increase in water temperature, which characterize marine heat waves, in temperate areas may enhance the autotrophic metabolism of seagrass communities and can yield an increase in the DOC released, in contrast to previous researches suggesting solely negative effects on seagrasses.

Effects of ocean acidification and hydrodynamic conditions on carbon metabolism and dissolved organic carbon (DOC) fluxes in seagrass populations.

Global change has been acknowledged as one of the main threats to the biosphere and its provision of ecosystem services, especially in marine ecosystems. Seagrasses play a critical ecological role in coastal ecosystems, but their responses to ocean acidification (OA) and climate change are not well understood. There have been previous studies focused on the effects of OA, but the outcome of interactions with co-factors predicted to alter during climate change still needs to be addressed. For example, the impact of higher CO2 and different hydrodynamic regimes on seagrass performance remains unknown. We studied the effects of OA under different current velocities on productivity of the seagrass Zostera noltei, using changes in dissolved oxygen as a proxy for the seagrass carbon metabolism, and release of dissolved organic carbon (DOC) in a four-week experiment using an open-water outdoor mesocosm. Under current pH conditions, increasing current velocity had a positive effect on productivity, but this depended on shoot density. However, this positive effect of current velocity disappeared under OA conditions. OA conditions led to a significant increase in gross production rate and respiration, suggesting that Z. noltei is carbon-limited under the current inorganic carbon concentration of seawater. In addition, an increase in non-structural carbohydrates was found, which may lead to better growing conditions and higher resilience in seagrasses subjected to environmental stress. Regarding DOC flux, a direct and positive relationship was found between current velocity and DOC release, both under current pH and OA conditions. We conclude that OA and high current velocity may lead to favourable growth scenarios for Z. noltei populations, increasing their productivity, non-structural carbohydrate concentrations and DOC release. Our results add new dimensions to predictions on how seagrass ecosystems will respond to climate change, with important implications for the resilience and conservation of these threatened ecosystems.

Latitudinal Patterns in European Seagrass Carbon Reserves: Influence of Seasonal Fluctuations versus Short-Term Stress and Disturbance Events.

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.

Global and local disturbances interact to modify seagrass palatability.

Global change, such as warming and ocean acidification, and local anthropogenic disturbances, such as eutrophication, can have profound impacts on marine organisms. However, we are far from being able to predict the outcome of multiple interacting disturbances on seagrass communities. Herbivores are key in determining plant community structure and the transfer of energy up the food web. Global and local disturbances may alter the ecological role of herbivory by modifying leaf palatability (i.e. leaf traits) and consequently, the feeding patterns of herbivores. This study evaluates the main and interactive effects of factors related to global change (i.e. elevated temperature, lower pH levels and associated ocean acidification) and local disturbance (i.e. eutrophication through ammonium enrichment) on a broad spectrum of leaf traits using the temperate seagrass Cymodocea nodosa, including structural, nutritional, biomechanical and chemical traits. The effect of these traits on the consumption rates of the generalist herbivore Paracentrotus lividus (purple sea urchin) is evaluated. The three disturbances of warming, low pH level and eutrophication, alone and in combination, increased the consumption rate of seagrass by modifying all leaf traits. Leaf nutritional quality, measured as nitrogen content, was positively correlated to consumption rate. In contrast, a negative correlation was found between feeding decisions by sea urchins and structural, biomechanical and chemical leaf traits. In addition, a notable accomplishment of this work is the identification of phenolic compounds not previously reported for C. nodosa. Our results suggest that global and local disturbances may trigger a major shift in the herbivory of seagrass communities, with important implications for the resilience of seagrass ecosystems.

Interaction between Ammonium Toxicity and Green Tide Development Over Seagrass Meadows: A Laboratory Study.

Eutrophication affects seagrasses negatively by increasing light attenuation through stimulation of biomass of fast-growing, bloom-forming algae and because high concentrations of ammonium in the water can be toxic to higher plants. We hypothesized nevertheless, that moderate amounts of nitrophilic macroalgae that coexists with seagrasses under eutrophic conditions, can alleviate the harmful effects of eutrophication on seagrasses by reducing ammonium concentrations in the seawater to non-toxic levels because such algae have a very large capacity to take up inorganic nutrients. We studied therefore how combinations of different ammonium concentrations (0, 25 and 50 µM) and different standing stocks of macroalgae (i.e. 0, 1 and 6 layers of Ulva sp.) affected survival, growth and net production of the seagrass Zostera noltei. In the absence of Ulva sp., increasing ammonium concentrations had a negative influence on the performance of Z. noltei. The presence of Ulva sp. without ammonium supply had a similar, but slightly smaller, negative effect on seagrass fitness due to light attenuation. When ammonium enrichment was combined with presence of Ulva sp., Ulva sp. ameliorated some of negative effects caused by high ammonium availability although Ulva sp. lowered the availability of light. Benthic microalgae, which increased in biomass during the experiment, seemed to play a similar role as Ulva sp.--they contributed to remove ammonium from the water, and thus, aided to keep the ammonium concentrations experienced by Z. noltei at relatively non-toxic levels. Our findings show that moderate amounts of drift macroalgae, eventually combined with increasing stocks of benthic microalgae, may aid seagrasses to alleviate toxic effects of ammonium under eutrophic conditions, which highlights the importance of high functional diversity for ecosystem resistance to anthropogenic disturbance.

Interactions between seagrass complexity, hydrodynamic flow and biomixing alter food availability for associated filter-feeding organisms.

Seagrass shoots interact with hydrodynamic forces and thereby a positively or negatively influence the survival of associated species. The modification of these forces indirectly alters the physical transport and flux of edible particles within seagrass meadows, which will influence the growth and survivorship of associated filter-feeding organisms. The present work contributes to gaining insight into the mechanisms controlling the availability of resources for filter feeders inhabiting seagrass canopies, both from physical (influenced by seagrass density and patchiness) and biological (regulated by filter feeder density) perspectives. A factorial experiment was conducted in a large racetrack flume, which combined changes in hydrodynamic conditions, chlorophyll a concentration in the water and food intake rate (FIR) in a model active filter-feeding organism (the cockle). Results showed that seagrass density and patchiness modified both hydrodynamic forces and availability of resources for filter feeders. Chlorophyll a water content decreased to 50% of the initial value when densities of both seagrass shoots and cockles were high. Also, filter feeder density controlled resource availability within seagrass patches, depending on its spatial position within the racetrack flume. Under high density of filter-feeding organisms, chlorophyll a levels were lower between patches. This suggests that the pumping activity of cockles (i.e. biomixing) is an emergent key factor affecting both resource availability and FIR for filter feeders in dense canopies. Applying our results to natural conditions, we suggest the existence of a direct correlation between habitat complexity (i.e. shoot density and degree of patchiness) and filter feeders density. Fragmented and low-density patches seem to offer both greater protection from hydrodynamic forces and higher resource availability. In denser patches, however, resources are allocated mostly within the canopy, which would benefit filter feeders if they occurred at low densities, but would be limiting when filter feeder were at high densities.

Clonal extent, apical dominance and networking features in the phalanx angiosperm Zostera noltii Hornem.

Disaggregating seagrass meadows and studying its components separately (clones, ramets, shoots) can provide us insights on meadow dynamics and growth patterns. The clonal growth, dependent upon clonal rules may regulate and impose constraints to plant architecture and, therefore, determine how individual clones evolve into the environment. In order to investigate the relationship between clonal growth rules and clone architecture, the belowground network architecture of single-clones of the seagrass Zostera noltii was studied. Networks were traced in situ after washing out the overlying sediment, and network characteristics were measured using digital analysis: area covered by clone, total rhizome length, type of rhizomatic axes (main, secondary, tertiary, quaternary), number and length of the internodes, branching angles and branching frequencies. This approach revealed that Z. noltii is able to develop into large clones integrating up to 300 internodes, 676 cm of rhizome, 208 shoots and 4,300 cm2 of plant area. Internodal length depended on both, the distance to the apical shoot (time effect) and the axes type (apical dominance effect). However, average branching angle was independent of axis type (average 58.3 ± 0.75), but varied significantly depending on the distance from the apical shoot. This average branching angle allows Z. noltii maximize the rate of centrifugal expansion, maintaining a high density in colonized areas to produce close stands but also minimizing the investment in belowground biomass and ramets overlapping. The clonal architecture of Z. noltii seems to be regulated by the interaction of both, apical dominance strength and clonal integration distance. Moreover, clonal growth rules and growth pattern seem to constrain clonality through (clonal) plant architecture regulations (i.e. branching is restricted in secondary axes, similar average branching angles regardless the axes, the higher the distance to the apex the higher the number of internodes in secondary axes, shorter internodes in secondary and tertiary axes). Future research efforts should focus on how these complex relationships between apical dominance and clonal integration interact to elucidate the temporal (seasonal) and spatial scales of both processes and the outcome at the plant architectural level.

Fire, rain and the selection of seeder and resprouter life-histories in fire-recruiting, woody plants.

Several Cape species of the genus Erica are known to present seeder and resprouter phenotypes, and this variation seems to have a genetic basis. Therefore, this genus provides ideal model systems for using to elucidate the evolution of nonsprouting or seeder and resprouter life-histories in woody, fire-recruiting plants. A simple simulation model was developed to identify, under life-history optimality, the ecological conditions (viz. rainfall conditions and fire frequency) that conferred a selective advantage to the seeder phenotype over the resprouter in a given Cape Erica species. The model illustrated that the seeder life-history was able to invade and replace a resprouter population only under a mild mediterranean climate, with short, moderate summer droughts. This simulation approach will contribute to a better understanding of the biogeographical pattern of seeder and resprouter lineages of one of the paradigmatic fynbos woody taxa throughout the Cape floristic region.

Growth, carbon allocation and proteolytic activity in the seagrass Zostera noltii shaded by Ulva canopies.

The effects of light reduction [100%, 25%, 10% and 1% mean daily-integrated photon irradiance (I0)] by Ulva rigida C. Agardh canopies on carbon balance, sugar-related enzymes and proteolytic activities of the seagrass Zostera noltii Hornem. were investigated. Shaded plants showed negative net growth and starch was mobilized in both above- and below-ground tissues. Sucrose declined in below-ground parts under severe light deprivation (10% and 1% I0), but was accumulated in above-ground parts. Mobilization of the non-structural carbohydrates (sucrose and starch) was explained by changes in activities of sucrose synthase (SuSy, EC 2.4.1.13) and sucrose-phosphate synthase (SPS, EC 2.4.2.24). Under severe light reduction, the capacity of above-ground tissues for sucrose formation and export declined, indicated by the lowest SPS activity. In contrast, severe light reduction increased the 'sink strength' of below-ground tissues, demonstrated by the highest SuSy activities, and diminished the capacity for sucrose resynthesis from starch breakdown, as the lowest SPS activity was observed under low light. These results suggest a cessation of sucrose transport throughout the plant under extreme light limitation, the carbon supply being dependent on the starch breakdown in each tissue. The response of Z. noltii to gradual light reduction was co-ordinated at the whole-plant level, since an enhancement of proteolytic activities induced by carbon starvation in both above- and below-ground tissues was also recorded during prolonged light deprivation. Therefore, carbon mobilization was accompanied by enhanced protein turnover and changes in metabolic pathways.