Soundscape analysis can be an effective tool in assessing seagrass restoration early success.

Restoration of vulnerable marine habitats is becoming increasingly popular to cope with widespread habitat loss and the resulting decline in biodiversity and ecosystem services. Lately, restoration strategies have been employed to enhance the recovery of degraded meadows of the Mediterranean endemic seagrass Posidonia oceanica. Typically, habitat restoration success is evaluated by the persistence of foundation species after transplantation (e.g., plant survival and growth) on the short and long-term, although successful plant responses do not necessarily reflect the recovery of ecosystem biodiversity and functions. Recently, soundscape (the spatial, temporal and frequency attribute of ambient sound and types of sound sources characterizing it) has been related to different habitat conditions and community structures. Thus, a successful restoration action should lead to acoustic restoration and soundscape ecology could represent an important component of restoration monitoring, leading to assess successful habitat and community restoration. Here, we evaluated acoustic community and metrics in a P. oceanica restored meadow and tested whether the plant transplant effectiveness after one year was accompanied by a restored soundscape. With this goal, acoustic recordings from degraded, transplanted and reference meadows were collected in Sardinia (Italy) using passive acoustic monitoring devices. Soundscape at each meadow type was examined using both spectral analysis and classification of fish calls based on a catalogue of fish sounds from the Mediterranean Sea. Seven different fish sounds were recorded: most of them were present in the reference and transplanted meadows and were associated to Sciaena umbra and Scorpaena spp. Sound Pressure Level (SPL, in dB re: 1 µPa-rms) and Acoustic Complexity Index (ACI) were influenced by the meadow type. Particularly higher values were associated to the transplanted meadow. SPL and ACI calculated in the 200-2000 Hz frequency band were also related to high abundance of fish sounds (chorus). These results showed that meadow restoration may lead to the recovery of soundscape and the associated community, suggesting that short term acoustic monitoring can provide complementary information to evaluate seagrass restoration success.

Salinity stress on three representative species from Mediterranean semifixed dunes: Assessment of salinity exposure and substrate conductivity data reveal variable response strategies and tolerance between species.

Coastal ecotones can disrupt natural conditions, yielding intricate ecological contexts where salinity plays a variable role. The aim of this study was to assess the salinity effect on three species representatives of semifixed dune (Crucianella maritima, Helianthemum caput-felis and Teucrium dunense). Field data were collected to assess plant cover in semifixed dunes, ecotone with other coastal habitats, and artificial Posidonia oceanica wracks. Soil samples were collected, and conductivity measured. Then, experimental exposure to salinity was conducted with 6 seawater (SW) treatments (Control, 6.25 % SW, 12.5 % SW, 25 % SW, 50 % SW, 100 % SW). Flowering, gas exchange, chlorophyll fluorescence and enzymatic antioxidant measurements were conducted after two months of exposure. In the field trial, species presence varied depending on the habitat and was null on P. oceanica. The relation between conductivity and species abundance showed moderate tolerance for the three species. For C. maritima this relation was variable depending on the habitat. Experimental data suggest moderate tolerance with stress occurring at 25 % SW onwards. Gas exchange response to salinity was similar among species, but more drastic reduction in assimilation rate and larger decrease in water use efficiency was observed for C. maritima. Instead, photoinhibition occurred in H. caput-felis and T. dunense but was absent in C. maritima likely related to the fact that H. caput-felis and T. dunense activated catalase and superoxide dismutase enzymes, while C. maritima showed activation of glutathione-related enzymes. Malondialdehyde (MDA) increased in C. maritma and decreased for the other species indicating a more complex involvement of MDA under stress conditions. Flowering response to salinity was overall more resilient in T. dunense. Our results, based on field conductivity data and measurements of physiological, antioxidant, and reproductive traits, delineate specific tolerance differences and strategies towards salinity for Mediterranean semifixed dune species.

How the seagrass Posidonia oceanica flowering will benefit from climate change.

This study aimed at identifying the importance of the thermal framework preceding Posidonia oceanica flowering induction (autumn before the flowering year) and anthesis (summer of the flowering year). In 53 locations of Sardinia (Italy), 35 vertical shoots were collected in 2001, 2020 and 2023 and analyzed through lepidochronology, detecting past flowering events from 1991 to 2022. Flowering probability was positively correlated with autumn SST range and MHWs, stressing the importance of the temperature in the year preceding the flowering. Summer SST mean and Marine Cold Spell duration (the latter emerged as a novel outcome) also positively influenced flowering. A negative association was highlighted with the summer SST range. As the occurrence of MHWs will increase, and the SST range will also increase in the autumn and decrease in the summer, P. oceanica might benefit through a higher flowering frequency, leading to a greater resilience to disturbances due to higher genetic variation.

Nutrient enrichment and herbivory alter carbon balance in temperate seagrass communities.

Large nutrient levels and herbivory stress, particularly when acting together, drive a variety of responses in seagrass communities that ultimately may weaken their carbon balance. An in situ three-months experiment was carried out in two contrasting seasons to address the effects of two levels of nutrient load and three levels of artificial clipping on Cymodocea nodosa plants. Nutrient enrichment shifted the community from autotrophic to heterotrophic and reduced DOC fluxes in winter, whereas enhanced community carbon metabolism and DOC fluxes in summer. Herbivory stress decreased the net primary production in both seasons, whereas net DOC release increased in winter but decreased in summer. A reduction of seagrass food-web structure was observed under both disturbances evidencing impacts on the seagrass ecosystems services by altering the carbon transfer process and the loss of superficial OC, which may finally weaken the blue carbon storage capacity of these communities.

Speeding up the recovery of coastal habitats through management interventions that address constraints on dispersal and recruitment.

Plans for habitat restoration will benefit from predictions of timescales for recovery. Theoretical models have been a powerful tool for informing practical guidelines in planning marine protected areas, suggesting restoration planning could also benefit from a theoretical framework. We developed a model that can predict recovery times following restoration action, under dispersal, recruitment and connectivity constraints. We apply the model to a case study of seagrass restoration and find recovery times following restoration action can vary greatly, from <1 to >20 years. The model also shows how recovery can be accelerated when restoration actions are matched to the constraints on recovery. For example, spreading of propagules can be used when connectivity is the critical restriction. The recovery constraints we articulated mathematically also apply to the restoration of coral reefs, mangroves, saltmarsh, shellfish reefs and macroalgal forests, so our model provides a general framework for choosing restoration actions that accelerate coastal habitat recovery.

Sub-lethal effects of metal(loid) contamination on the halophyte Sarcocornia quinqueflora with links to plant photosynthetic performance and biomass - A field study.

Two saltmarsh locations within Lake Macquarie, NSW, Australia were selected to investigate the uptake and partitioning of metal(loid)s Cu, Zn, As, Se, Cd and Pb in the Australian saltmarsh halophyte, Sarcocornia quinqueflora and the associated sub-lethal effects of metal(loid)s on plant health, including photosynthetic performance, biomass, and productivity. Metal(loid)s primarily accumulated to roots (BCF > 1). Barriers to transport were observed at the root to non-photosynthetic stem transition (TF < 1) for all metal(loid)s, suggesting this species is suitable for phytostabilisation. Sediment and plant tissue metal(loid) concentrations were significantly correlated with photosynthetic performance and plant biomass. As such, the action of sediment and tissue metal(loid)s on photosynthetic performance and the subsequent effect on biomass of S.quinqueflora appear to be suitable targets for molecular analyses to further elucidate mechanisms responsible for the observed adverse effects and the development of adverse outcome pathways.

Resistance of Posidonia oceanica seedlings to warming: Investigating the importance of the lag-phase duration between two heat events to thermo-priming.

The increase of marine heat waves (MHWs) occurrence is exacerbated in Mediterranean Sea and temperature resilience-enhancing strategies on key species, such as the seagrass Posidonia oceanica, need to be investigated. "Priming" describes a stimulus that prepares an organism for an improved response to upcoming environmental changes by triggering a memory that remains during a lag-phase. The aim of this study, conducted in Sardinia (Italy), was to investigate whether the development of thermo-primed P. oceanica seedlings is affected by a field simulated MHW depending on the duration of the lag-phase. After the thermo-priming stimulus, seedlings had a 0, 7 or 14 days lag-phase and after that, for each lag-phase group, half of the seedlings experienced a simulated MHW (the other half served as controls). Some other seedlings did not experience either the priming stimulus or the lag-phase. Results did not show any evidence of a memory triggered by the priming stimulus, but they highlighted the importance of an acclimation phase before the highest temperature: seedlings that experienced a gradual increase of temperature had a higher number of leaves and shorter leaf necrosis length compared to seedlings that had a lag-phase between two heat events. Regardless the priming stimulus, MHWs slowed down the development of the leaf and root length. Considering the increase of temperature fluctuations, testing different intensities of priming and different length of lag-phase is necessary to provide information about the adaptive success of the species.

Mass flowering and unprecedented extended pseudovivipary in seagrass (Posidonia oceanica) after a Marine Heat Wave.

Seagrasses are marine flowering plants that create critical coastal ecosystems and are threatened by warming. Clonal expansion is generally the dominant strategy for meadow recovery, while sexual reproduction strongly differs among species (e.g., monoecious and diecious species, some creating seed banks, viviparous seedlings). In 2022, the Western Mediterranean underwent unprecedented warming, and, associated with it, we observed flowering (100 %) across 11 Posidonia oceanica meadows in Mallorca, Balearic Islands. Furthermore, 64 % of the sites also exhibited pseudovivipary, an extremely rare phenomenon in angiosperms whereby plantlets replace sexual reproductive structures, producing clones of the maternal plant. Our results support the notion that P. oceanica flowering and pseudovivipary (genetically confirmed) are triggered by warming, never before being pseudovivipary reported across multiple sites in a marine plant. Considering the negative impacts that warming can have on seagrasses, existence of widespread pseudovivipary is a critical aspect to consider for understanding mechanisms of resilience in seagrasses.

Effects of coastal development on sawfish movements and the need for marine animal crossing solutions.

Although human-made barriers to animal movement are ubiquitous across many types of ecosystems, the science behind these barriers and how to ameliorate their effects lags far behind in marine environments compared with terrestrial and freshwater realms. Using juvenile sawfish in an Australian nursery habitat as a model system, we aimed to assess the effects of a major anthropogenic development on the movement behavior of coastal species. We compared catch rates and movement behavior (via acoustic telemetry) of juvenile green sawfish (Pristis zijsron) before and after a major coastal structure was built in an important nursery habitat. Acoustic tracking and catch data showed that the development did not affect levels of sawfish recruitment in the nursery, but it did constrain movements of juveniles moving throughout the nursery, demonstrating the reluctance of shoreline-associated species to travel around large or unfamiliar coastal structures. Given the current lack of information on human-made movement barriers in the marine environment, these findings highlight the need for further research in this area, and we propose the development of and experimentation with marine animal crossings as an important area of emerging research.

Efectos del desarrollo costero sobre los movimientos del pez sierra y la necesidad de soluciones para el cruce de animales marinos Resumen Mientras que las barreras construidas por humanos que limitan el movimiento de animales son ubicuas en muchos tipos de ecosistemas, la ciencia que sustenta estas barreras y la reducción de sus impactos está muy retrasada en ambientes marinos en comparación con medios terrestres y dulceacuícolas. Utilizando peces sierra juveniles en un hábitat de vivero australiano como sistema modelo, intentamos evaluar los efectos de un importante desarrollo antropogénico sobre el comportamiento de especies costeras. Comparamos las tasas de captura y el comportamiento de movimiento (mediante telemetría acústica) de peces sierra verdes juveniles (Pristis zijsron) antes y después de que se construyera infraestructura costera en un importante hábitat de vivero. El seguimiento acústico y los datos de captura mostraron que el desarrollo no afectó los niveles de reclutamiento de pez sierra en el vivero, pero sí restringió los movimientos de los juveniles desplazándose por el vivero, lo cual demuestra la renuencia de las especies asociadas a la costa a viajar alrededor de estructuras costeras grandes o desconocidas. Dada la actual falta de información sobre las barreras de movimiento creadas por el hombre en el medio marino, estos hallazgos destacan la necesidad de realizar más investigaciones en esta campo, y proponemos el desarrollo y la experimentación con cruces para animales marinos como un área importante de investigación emergente.

Spatial signatures of an approaching regime shift in Posidonia oceanica meadows.

Determining the proximity of ecosystems to tipping points is a critical yet complex task, heightened by the growing severity of climate change and local anthropogenic stressors on ecosystem integrity. Spatial Early Warning Signals (EWS) have been recognized for their potential in preemptively signaling regime shifts to degraded states, but their performance in natural systems remains uncertain. In this study, we investigated the performance of 'recovery length' - the spatial extent of recovery from a perturbation - and spatial EWS as early warnings of regime shifts in Posidonia oceanica meadows. Our experimental approach involved progressively thinning the P. oceanica canopy, from 0 to 100%, at the edge of a dead-matte area - a structure formed by dead P. oceanica rhizomes and colonized by algal turfs - to promote the propagation of algal turfs. We calculated recovery length as the distance from the dead-matte edge to the point where algal turfs colonized the canopy-thinned region. Our results showed a linear increase in recovery length with canopy thinning, successfully anticipated the degradation of P. oceanica. While spatial skewness decline with increased canopy degradation, other spatial EWS, such as Moran correlation at lag-1, low-frequency spatial spectra, and spatial variance, were ineffective in signaling this degradation. These findings underscore the potential of recovery length as a reliable early warning indicator of regime shifts in marine coastal ecosystems.

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.

Early signals of Posidonia oceanica meadows recovery in a context of wastewater treatment improvements.

Natural ecological restoration is a cornerstone of modern conservation science and managers need more documented "success stories" to lead the way. In French mediterranean sea, we monitored Posidonia oceanica lower limit using acoustic telemetry and photogrammetry and investigated the descriptors driving its variations, at a national scale and over more than a decade. We showed significant effects of environmental descriptors (region, sea surface temperature and bottom temperature) but also of wastewater treatment plant (WWTP) effluents proxies (size of WWTP, time since conformity, and distance to the closest effluent) on the meadows lower limit progression. This work indicates a possible positive response of P. oceanica meadows to improvements in wastewater treatment and a negative effect of high temperatures. While more data is needed, the example of French wastewater policy should inspire stakeholders and coastal managers in their efforts to limit anthropogenic pressures on vulnerable ecosystems.

Transcriptomic profiles and diagnostic biomarkers in the Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa reveal mechanistic insights of adaptative strategies upon desalination brine stress.

Seawater desalination by reverse osmosis is growing exponentially due to water scarcity. Byproducts of this process (e.g. brines), are generally discharged directly into the coastal ecosystem, causing detrimental effects, on benthic organisms. Understanding the cellular stress response of these organisms (biomarkers), could be crucial for establishing appropriate salinity thresholds for discharged brines. Early stress biomarkers can serve as valuable tools for monitoring the health status of brine-impacted organisms, enabling the prediction of long-term irreversible damage caused by the desalination industry. In this study, we conducted laboratory-controlled experiments to assess cellular and molecular biomarkers against brine exposure in two salinity-sensitive Mediterranean seagrasses: Posidonia oceanica and Cymodocea nodosa. Treatments involved exposure to 39, 41, and 43 psu, for 6 h and 7 days. Results indicated that photosynthetic performance remained unaffected across all treatments. However, under 43 psu, P. oceanica and C. nodosa exhibited lipid oxidative damage, which occurred earlier in P. oceanica. Additionally, P. oceanica displayed an antioxidant response at higher salinities by accumulating phenolic compounds within 6 h and ascorbate within 7 d; whereas for C. nodosa the predominant antioxidant mechanisms were phenolic compounds accumulation and total radical scavenging activity, which was evident after 7 d of brines exposure. Finally, transcriptomic analyses in P. oceanica exposed to 43 psu for 7 days revealed a poor up-regulation of genes associated with brassinosteroid response and abiotic stress response, while a high down-regulation of genes related to primary metabolism was detected. In C. nodosa, up-regulated genes were involved in DNA repair, cell cycle regulation, and reproduction, while down-regulated genes were mainly associated with photosynthesis and ribosome assembly. Overall, these findings suggest that 43 psu is a critical salinity-damage threshold for both seagrasses; and despite the moderate overexpression of several transcripts that could confer salt tolerance, genes involved in essential biological processes were severely downregulated.

Ocean acidification impairs seagrass performance under thermal stress in shallow and deep water.

Despite the effects of ocean acidification (OA) on seagrasses have been widely investigated, predictions of seagrass performance under future climates need to consider multiple environmental factors. Here, we performed a mesocosm study to assess the effects of OA on shallow and deep Posidonia oceanica plants. The experiment was run in 2021 and repeated in 2022, a year characterized by a prolonged warm water event, to test how the effects of OA on plants are modulated by thermal stress. The response of P. oceanica to experimental conditions was investigated at different levels of biological organization. Under average seawater temperature, there were no effects of OA in both shallow and deep plants, indicating that P. oceanica is not limited by current inorganic carbon concentration, regardless of light availability. In contrast, under thermal stress, exposure of plants to OA increased lipid peroxidation and decreased photosynthetic performance, with deep plants displaying higher levels of heat stress, as indicated by the over-expression of stress-related genes and the activation of antioxidant systems. In addition, warming reduced plant growth, regardless of seawater CO2 and light levels, suggesting that thermal stress may play a fundamental role in the future development of seagrass meadows. Our results suggest that OA may exacerbate the negative effects of future warming on seagrasses.

Anchoring pressure and the effectiveness of new management measures quantified using AIS data and a mobile application.

Large boats can have a major impact on sensitive marine habitats like seagrass meadows when anchoring. The anchoring preference of large boats and their impacts can be mapped using Automatic Identification System (AIS). We found a constant increase in the number of anchoring events with, until recently, a large part of them within the protected Posidonia oceanica seagrass meadows. French authorities adopted a new regulation in 2019 forbidding any anchoring within P. oceanica seagrass meadows for boats larger than 24 m. The number of large ships (>24 m) anchoring in P. oceanica meadows significantly decreased after the enforcement of the regulation. The surface of avoided impact thanks to the new regulation corresponds to 134 to 217 tons of carbon sequestered by the preserved meadow in 2022. This work illustrates that a strict regulation of anchoring, based on accurate habitat maps, is effective in protecting seagrass meadows.

Unexpected slow recovery of seagrass leaf epiphytes after the impact of a summer heat wave and concomitant mucilage bloom.

The epiphytes of seagrass leaves constitute a peculiar community, comprised of a number of species specialized for this living substrate. Several studies report on the response of epiphytes to different pressures but no information exists about the effects of summer heatwaves, which have become frequent events in the last decades. This paper represents the first attempt to investigate the change in the leaf epiphyte community of the Mediterranean seagrass Posidonia oceanica due to the heatwave occurred in summer 2003. Thanks to a series of data collected seasonally between 2002 and 2006, and punctual data in the summers of 2014 and 2019, we assessed the change over time in the leaf epiphyte community. Temperature data trends were analysed through linear regression, while multivariate analyses (i.e., nMDS and SIMPER) were applied to cover data in order to assess changes over time in the epiphyte community. As a whole, the two most abundant taxa were the crustose coralline alga Hydrolithon and the encrusting bryozoan Electra posidoniae, which displayed the highest average cover values in summer (around 19%) and spring (around 9%), respectively. Epiphytes proved to be sensitive to temperature highs, displaying different effects on cover, biomass, diversity and community composition. Cover and biomass exhibited a dramatic reduction (more than 60%) after the disturbance. In particular, Hydrolithon more than halved, while E. posidoniae dropped sevenfold during summer 2003. While the former recovered comparatively quickly, the latter, as well as the whole community composition, apparently required 16 years to return to a condition similar to that of 2002.

Sources of variability in seagrass fatty acid profiles and the need of identifying reliable warming descriptors.

Global warming is expected to have inexorable and profound effects on marine ecosystems, particularly in foundation species such as seagrasses. Identifying responses to warming and comparing populations across natural temperature gradients can inform how future warming will impact the structure and function of ecosystems. Here, we investigated how thermal environment, intra-shoot and spatial variability modulate biochemical responses of the Mediterranean seagrass Posidonia oceanica. Through a space-for-time substitution study, Fatty acid (FA) profiles on the second and fifth leaf of the shoots were quantified at eight sites in Sardinia along a natural sea surface temperature (SST) summer gradient (about 4 °C). Higher mean SST were related to a decrease in the leaf total fatty acid content (LTFA), a reduction in polyunsaturated fatty acids (PUFA), omega-3/omega-6 PUFA and PUFA/saturated fatty acids (SFA) ratios and an increase in SFA, monounsaturated fatty acids and carbon elongation index (CEI, C18:2 n-6/C16:2 n-6) ratio. Results also revealed that FA profiles were strongly influenced by leaf age, independently of SST and spatial variability within sites. Overall, this study evidenced that the sensitive response of P. oceanica FA profiles to intra-shoot and spatial variability must not be overlooked when considering their response to temperature changes.

Rise of Ruppia in Chesapeake Bay: Climate change-driven turnover of foundation species creates new threats and management opportunities.

Global change has converted many structurally complex and ecologically and economically valuable coastlines to bare substrate. In the structural habitats that remain, climate-tolerant and opportunistic species are increasing in response to environmental extremes and variability. The shifting of dominant foundation species identity with climate change poses a unique conservation challenge because species vary in their responses to environmental stressors and to management. Here, we combine 35 y of watershed modeling and biogeochemical water quality data with species comprehensive aerial surveys to describe causes and consequences of turnover in seagrass foundation species across 26,000 ha of habitat in the Chesapeake Bay. Repeated marine heatwaves have caused 54% retraction of the formerly dominant eelgrass (Zostera marina) since 1991, allowing 171% expansion of the temperature-tolerant widgeongrass (Ruppia maritima) that has likewise benefited from large-scale nutrient reductions. However, this phase shift in dominant seagrass identity now presents two significant shifts for management: Widgeongrass meadows are not only responsible for rapid, extensive recoveries but also for the largest crashes over the last four decades; and, while adapted to high temperatures, are much more susceptible than eelgrass to nutrient pulses driven by springtime runoff. Thus, by selecting for rapid post-disturbance recolonization but low resistance to punctuated freshwater flow disturbance, climate change could threaten the Chesapeake Bay seagrass' ability to provide consistent fishery habitat and sustain functioning over time. We demonstrate that understanding the dynamics of the next generation of foundation species is a critical management priority, because shifts from relatively stable habitat to high interannual variability can have far-reaching consequences across marine and terrestrial ecosystems.

Effect of shading imposed by the algae Chaeotomorpha linum loads on structure, morphology and physiology of the seagrass Cymodocea nodosa.

In shallow coastal waters, seagrass and macroalgae occur together but under eutrophic conditions, bloom-forming algae can take over seagrasses causing an irreversible regime shift. Understanding the effect of macroalgae loads on seagrass meadows at an early stage can help prevent the loss of these ecosystems and the services they provide. In the present study, in situ experiments were conducted for 90 days in Bekalta (eastern coast of Tunisia) to assess the response of the seagrass Cymodocea nodosa when challenged with shading induced by filamentous macroalgae Chaetomorpha linum. Structural, morphological and physiological variables were regularly measured during the experiment. Shaded plants showed a sharp decline in shoot density, growth rate, and above-ground biomass, the impact being more pronounced on the physiological traits. Besides, shading by C. linum induced a significant increase in the contents of leaf photosynthetic pigments and phenolic compounds, whereas causing a decrease in soluble protein and sugar concentrations. Thus, shading imposed by C. linum loads appeared to induce a phoadpatative response in C. nodosa concomitant with carbon mobilization.