The resilience of transplanted seagrass traits encourages detection of restoration success.

Restoration of coastal ecosystems, particularly those dominated by seagrasses, has become a priority to recover the important ecosystem services they provide. However, assessing restoration outcomes as a success or failure remains still difficult, probably due to the unique features of seagrass species and the wide portfolio of practices used on transplanting actions. Here, several traits (maximum leaf length, number of leaves, leaf growth rate per shoot, and leaf elemental carbon and nitrogen contents) of transplanted seagrass Posidonia oceanica were compared to reference meadows in five sites of Western Mediterranean Sea in which restoration were completed in different times. Results have evidenced the resilience of transplanted P. oceanica shoots within a few years since restoration, as traits between treatments changed depending on the elapsed time since settlement. The highlighted stability of the restoration time effect suggests that the recovery of the plants is expected in four years after transplanting.

An integrated assessment of the Good Environmental Status of Mediterranean Marine Protected Areas.

Local, regional and global targets have been set to halt marine biodiversity loss. Europe has set its own policy targets to achieve Good Environmental Status (GES) of marine ecosystems by implementing the Marine Strategy Framework Directive (MSFD) across member states. We combined an extensive dataset across five Mediterranean ecoregions including 26 Marine Protected Areas (MPAs), their reference unprotected areas, and a no-trawl case study. Our aim was to assess if MPAs reach GES, if their effects are local or can be detected at ecoregion level or up to a Mediterranean scale, and which are the ecosystem components driving GES achievement. This was undertaken by using the analytical tool NEAT (Nested Environmental status Assessment Tool), which allows an integrated assessment of the status of marine systems. We adopted an ecosystem approach by integrating data from several ecosystem components: the seagrass Posidonia oceanica, macroalgae, sea urchins and fish. Thresholds to define the GES were set by dedicated workshops and literature review. In the Western Mediterranean, most MPAs are in good/high status, with P. oceanica and fish driving this result within MPAs. However, GES is achieved only at a local level, and the Mediterranean Sea, as a whole, results in a moderate environmental status. Macroalgal forests are overall in bad condition, confirming their status at risk. The results are significantly affected by the assumption that discrete observations over small spatial scales are representative of the total extension investigated. This calls for large-scale, dedicated assessments to realistically detect environmental status changes under different conditions. Understanding MPAs effectiveness in reaching GES is crucial to assess their role as sentinel observatories of marine systems. MPAs and trawling bans can locally contribute to the attainment of GES and to the fulfillment of the MSFD objectives. Building confidence in setting thresholds between GES and non-GES, investing in long-term monitoring, increasing the spatial extent of sampling areas, rethinking and broadening the scope of complementary tools of protection (e.g., Natura 2000 Sites), are indicated as solutions to ameliorate the status of the basin.

Seagrass collapse due to synergistic stressors is not anticipated by phenological changes.

Seagrasses are globally declining and often their loss is due to synergies among stressors. We investigated the interactive effects of eutrophication and burial on the Mediterranean seagrass, Posidonia oceanica. A field experiment was conducted to estimate whether shoot survival depends on the interactive effects of three levels of intensity of both stressors and to identify early changes in plants (i.e., morphological, physiological and biochemical, and expression of stress-related genes) that may serve to detect signals of imminent shoot density collapse. Sediment burial and nutrient enrichment produced interactive effects on P. oceanica shoot survival, as high nutrient levels had the potential to accelerate the regression of the seagrass exposed to high burial (HB). After 11 weeks, HB in combination with either high or medium nutrient enrichment caused a shoot loss of about 60%. Changes in morphology were poor predictors of the seagrass decline. Likewise, few biochemical variables were associated with P. oceanica survival (the phenolics, ORAC and leaf δ34S). In contrast, the expression of target genes had the highest correlation with plant survival: photosynthetic genes (ATPa, psbD and psbA) were up-regulated in response to high burial, while carbon metabolism genes (CA-chl, PGK and GADPH) were down-regulated. Therefore, die-offs due to high sedimentation rate in eutrophic areas can only be anticipated by altered expression of stress-related genes that may warn the imminent seagrass collapse. Management of local stressors, such as nutrient pollution, may enhance seagrass resilience in the face of the intensification of extreme climate events, such as floods.

Immanent conditions determine imminent collapses: nutrient regimes define the resilience of macroalgal communities.

Predicting where state-changing thresholds lie can be inherently complex in ecosystems characterized by nonlinear dynamics. Unpacking the mechanisms underlying these transitions can help considerably reduce this unpredictability. We used empirical observations, field and laboratory experiments, and mathematical models to examine how differences in nutrient regimes mediate the capacity of macrophyte communities to sustain sea urchin grazing. In relatively nutrient-rich conditions, macrophyte systems were more resilient to grazing, shifting to barrens beyond 1 800 g m-2 (urchin biomass), more than twice the threshold of nutrient-poor conditions. The mechanisms driving these differences are linked to how nutrients mediate urchin foraging and algal growth: controlled experiments showed that low-nutrient regimes trigger compensatory feeding and reduce plant growth, mechanisms supported by our consumer-resource model. These mechanisms act together to halve macrophyte community resilience. Our study demonstrates that by mediating the underlying drivers, inherent conditions can strongly influence the buffer capacity of nonlinear systems.

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.

Predation risk of the sea urchin Paracentrotus lividus juveniles in an overfished area reveal system stability mechanisms and restocking challenges.

Where sea urchin harvest has been so intense that populations have drastically regressed, concerns have arisen about the effectiveness of harvesting management. According to the theory of phase transition in shallow rocky reefs between vegetated and barren habitats, sea urchin recruitment, a key population structuring process, seems hampered by some stabilizing feedback despite an end to local human harvest of sea urchins. To shed a light on predation effects on sea urchin recruits, a 27-day field experiment was conducted using mega-predator exclusion cages (40x40x40 cm, 1 cm in mesh size) in barren and turf substrates. To facilitate this, 672 recruits (1.1 ± 0.02 cm in size) reared under control conditions were positioned in groups of 42 in each experimental unit (n = 4). Exclusion of mega-predators had a significant effect regardless the substrate, since a higher number of recruits was found under cages both in turf and barren. However, the results showed that in uncaged treatments the size of recruits that survived was larger in turf than in barren, as in the former substrate predation had reduced the abundance of the smallest recruits, highlighting that mega-predator presence affects differently the size of the recruits that had survived depending on the substrate. Overall, these results provide valuable information to address restocking actions of sea urchin populations in overharvested areas, where algal turfs are widespread, and assist studies on habitat stability mechanisms.

Areas of spatial overlap between common bottlenose dolphin, recreational boating, and small-scale fishery: management insights from modelling exercises.

Background: Sustainable management requires spatial mapping of both species distribution and human activities to identify potential risk of conflict. The common bottlenose dolphin (Tursiops truncatus) is a priority species of the European Union Habitat Directive, thus, to promote its conservation, the understanding of habitat use and distribution, as well as the identification and spatial trend of the human activities which may directly affect populations traits, is pivotal. Methods: A MaxEnt modeling approach was applied to predict the seasonal (from April to September) habitat use of a small population of bottlenose dolphins in the north-western Sardinia (Mediterranean Sea) in relation to environmental variables and the likelihoods of boat and fishing net presence. Then, the overlapping areas between dolphin, fishing net and boat presence were identified to provide insights for the marine spatial management of this area. Results: Three of the main factors influencing the seasonal distribution of bottlenose dolphins in the area are directly (boating and fishing) or indirectly (ocean warming) related to human activities. Furthermore, almost half of the most suitable area for dolphins overlapped with areas used by fishing and boating. Finally, relying on fishing distribution models, we also shed light on the potential impact of fishing on the Posidonia oceanica beds, a protected habitat, which received higher fishing efforts than other habitat types. Discussion: Modelling the spatial patterns of anthropogenic activities was fundamental to understand the ecological impacts both on cetacean habitat use and protected habitats. A greater research effort is suggested to detect potential changes in dolphin habitat suitability, also in relation to ocean warming, to assess dolphin bycatch and the status of target fish species, and to evaluate sensitive habitats conditions, such as the Posidonia oceanica meadow.

Cultivable mycoflora on bleached, decaying and healthy Posidonia oceanica leaves in a warm-edge Mediterranean location.

Marine fungi are widely distributed in the ocean, playing an important role in the ecosystems, but only little information is available about their occurrence and activity. Seagrass bleaching is also a neglected phenomenon that seems to be linked to warm environments, even though the causes are still to be defined. In this study, the cultivable mycoflora associated to the leaf conditions (bleached, necrotic and live) and section (from the base to the tip) in the seagrass Posidonia oceanica was investigated in a Mediterranean warm-edge location (Cyprus). A total of 17 Ascomycota species/taxon were identified and results highlighted that mycoflora composition changed significantly in relation to both the leaf condition and section. A few known pathogens of terrestrial plants were detected only on bleached leaves, but it remains unknown whether they have any direct connections with P. oceanica bleaching phenomenon.

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.

Field development of Posidonia oceanica seedlings changes under predicted acidification conditions.

Ocean acidification has been consistently evidenced to have profound and lasting impacts on marine species. Observations have shown seagrasses to be highly susceptible to future increased pCO2 conditions, but the responses of early life stages as seedlings are poorly understood. This study aimed at evaluating how projected Mediterranean Sea acidification affects the survival, morphological and biochemical development of Posidonia oceanica seedlings through a long-term field experiment along a natural low pH gradient. Future ocean conditions seem to constrain the morphological development of seedlings. However, high pCO2 exposures caused an initial increase in the degree of saturation of fatty acids in leaves and then improved the fatty acid adjustment increasing unsaturation levels in leaves (but not in seeds), suggesting a nutritional compound translocation. Results also suggested a P. oceanica structural components remodelling which may counteract the effects of ocean acidification but would not enhance seagrass seedling productivity.

Intensive sea urchin harvest rescales Paracentrotus lividus population structure and threatens self-sustenance.

The harvest of the edible sea urchin Paracentrotus lividus is intensively practiced in some regions of the Western Mediterranean Sea. The removal of the largest individuals can determine an overall reduction in population size and a size class truncation that can lead to a drastic drop the self-sustenance. The aim of this study is to evaluate the variability of the population reproductive potential across 5 years in one of the main harvest hotspots of Sardinia (Western Mediterranean Sea). The breeding stock consists of commercial and under-commercial size individuals which were sampled on a monthly basis to estimate their GonadoSomatic Index (GSI) and the Individual Gamete Output (IGO). In addition, the reproductive potential of the population-Total Gamete Output (TGO)-was calculated across the 5-year period in relation with the variation of the density of the breeding stock. During the last year, the reproductive potential was also estimated in a well-conserved population of a nearby Marine Protected Area. No significant variability in GSI and IGO was found over the 5 years nor when compared with the ones of protected population in the last year. However, the intensive harvest drastically rescaled the population body-size: although density of the commercial size class remained low, density of the under-commercial size-class halved from the beginning to the end of the study. Accordingly, the proportional decrease of their gamete output contribution led to a 40% loss of the reproductive potential of the whole population in the 5-year period. Interestingly, despite the loss of reproductive potential due to the decrease of the breeding stock density, the average values of IGO slightly increased across the years leading to the highest Annual Gamete Output (AGO) during the fourth year of sampling. This positive pattern could suggest a mechanism of reproductive investments of the survivors in terms of gonad production rate or increase in spawning intensity. This work provides evidence of the direct effect of size-selective harvesting on the rapid loss of population self-sustenance. Furthermore, it lays new prospective for future research of the indirect effects of the rescaling population body-size in functional traits of the sea urchin P. lividus and that could become important for both, sustainable exploitation and ecosystem conservation management.

Effects of high temperature and marine heat waves on seagrasses: Is warming affecting the nutritional value of Posidonia oceanica?

Primary producers nutritional content affects the entire food web. Here, changes in nutritional value associated with temperature rise and the occurrence of marine heat waves (MHWs) were explored in the endemic Mediterranean seagrass Posidonia oceanica. The variability of fatty acids (FAs) composition and carbon (C) and nitrogen (N) content were examined during summer 2021 from five Mediterranean sites located at the same latitude but under different thermal environments. The results highlighted a decrease in unsaturated FAs and C/N ratio and an increase of monounsaturated FA (MUFA) and N content when a MHW occurred. By contrast, the leaf biochemical composition seems to be adapted to local water temperature since only few significant changes in MUFA were found and N and C/N had an opposite pattern compared to when a MHW occurs. The projected increase in temperature and frequency of MHW suggest future changes in the nutritional value and palatability of leaves.

Nutrient conditions determine the strength of herbivore-mediated stabilizing feedbacks in barrens.

Abiotic environmental conditions can significantly influence the way species interact. In particular, plant-herbivore interactions can be substantially dependent on temperature and nutrients. The overall product of these relationships is critical for the fate and stability of vegetated ecosystems like marine forests. The last few decades have seen a rapid spread of barrens on temperate rocky reefs mainly as a result of overgrazing. The ecological feedbacks that characterize the barren state involve a different set of interactions than those occurring in vegetated habitats. Reversing these trends requires a proper understanding of the novel feedbacks and the conditions under which they operate. Here, we explored the role of a secondary herbivore in reinforcing the stability of barrens formed by sea urchin overgrazing under different nutrient conditions. Combining comparative and experimental studies in two Mediterranean regions characterized by contrasting nutrient conditions, we assessed: (i) if the creation of barren areas enhances limpet abundance, (ii) the size-specific grazing impact by limpets, and (iii) the ability of limpets alone to maintain barrens. Our results show that urchin overgrazing enhanced limpet abundance. The effects of limpet grazing varied with nutrient conditions, being up to five times more intense under oligotrophic conditions. Limpets were able to maintain barrens in the absence of sea urchins only under low-nutrient conditions, enhancing the stability of the depauperate state. Overall, our study suggests a greater vulnerability of subtidal forests in oligotrophic regions of the Mediterranean and demonstrates the importance of environment conditions in regulating feedbacks mediated by plant-herbivore interactions.

Collating evidence on the restoration efforts of the seagrass Posidonia oceanica: current knowledge and gaps.

Seagrass meadows are important shallow coastal ecosystems due to their contribution to enhancing biodiversity, nutrient cycling, carbon burial, and sediment stabilisation, but the maintenance of their integrity has been threatened by several anthropogenic disturbances. Active restoration is considered a reliable strategy to enhance recovery of seagrass ecosystems, and decision making for correct seagrass restoration management requires relying on valuable information regarding the effectiveness of past restoration actions and experimental efforts. Previous experimental efforts and human-mediated active restoration actions of the slow growing seagrass Posidonia oceanica have been collated here by combining a literature systematic review and questionnaires consulting seagrass ecology experts. Overall, the poor consistency of the available information on P. oceanica restoration may be due to the wide portfolio of practices and methodologies used in different conditions, that supports the need of further field manipulative experiments in various environmental contexts to fill the identified knowledge gaps. The current situation requires an international, collaborative effort from scientists and stakeholders to jointly design the future strategy forward in identifying the best practices that lead to efficient restorations of P. oceanica habitat and functioning.

Effects of Field Simulated Marine Heatwaves on Sedimentary Organic Matter Quantity, Biochemical Composition, and Degradation Rates.

Since rising temperature (T) will enhance biochemical reactions and coastal marine sediments are hotspots of carbon cycling, marine heatwaves' (MHWs') intensification caused by climate change will affect coastal biogeochemistry. We investigated the effects of MHWs on sediment organic matter (OM) in a nearshore locality (NW Sardinia, Mediterranean Sea) receiving an artificial warm water plume generating T anomalies of 1.5-5.0 °C. Sediments were collected before and after 3 and 11 weeks from the initial plume release. Both MHWs influenced sedimentary OM quantity, composition, and degradation rates, with major effects associated with the highest T anomaly after 3 weeks. Both MHWs enhanced sedimentary OM contents, with larger effects associated with the highest T anomaly. Phytopigment contents increased in the short term but dropped to initial levels after 11 weeks, suggesting the occurrence of thermal adaptation or stress of microphytobenthos. In the longer term we observed a decrease in the nutritional quality of OM and a slowdown of its turnover mediated by extracellular enzymes, suggestive of a decreased ecosystem functioning. We anticipate that intensification of MHWs will affect benthic communities not only through direct effects on species tolerance but also by altering benthic biogeochemistry and the efficiency of energy transfer towards higher trophic levels.

Field thermo acclimation increases the resilience of Posidonia oceanica seedlings to marine heat waves.

Acclimation is a response that results from chronic exposure of an individual to a new environment. This study aimed to investigate whether the thermal environment affects the early development of the seagrass Posidonia oceanica, and whether the effects of a field-simulated Marine Heat Wave (MHW) on seedlings change depending on acclimation. The experiment was done in the field using a crossed design of Acclimation (acclimated vs unacclimated) and MHW (present vs absent) factors. Acclimation has initially constrained the development of P. oceanica seedlings, but then it increased their resilience to the MHW, under both a morphological and biochemical (fatty acid saturation) level. This treatment could be considered in P. oceanica restoration projects in a climate change-impaired sea, by purposely inducing an increased resistance to heat before transplants.

Determinants of variability in signature whistles of the Mediterranean common bottlenose dolphin.

One of the most studied aspects of animal communication is the acoustic repertoire difference between populations of the same species. While numerous studies have investigated the variability of bottlenose dolphin whistles between populations, very few studies have focused on the signature whistles alone and the factors underlying differentiation of signature whistles are still poorly understood. Here we describe the signature whistles produced by six distinct geographical units of the common bottlenose dolphin (Tursiops truncatus) in the Mediterranean Sea and identify the main determinants of their variability. Particularly, the influence of the region (proxy of genetic distance), the geographic site, and the environmental (sea bottom-related) and demographical (population-related) conditions on the acoustic structure of signature whistles was evaluated. The study provides the first evidence that the genetic structure, which distinguishes the eastern and western Mediterranean bottlenose dolphin populations has no strong influence on the acoustic structure of their signature whistles, and that the geographical isolation between populations only partially affected whistle variability. The environmental conditions of the areas where the whistles developed and the demographic characteristics of the belonging populations strongly influenced signature whistles, in accordance with the "acoustic adaptation hypothesis" and the theory of signature whistle determination mediated by learning.

Sea urchin harvest inside marine protected areas: an opportunity to investigate the effects of exploitation where trophic upgrading is achieved.

Background: Marine protected areas (MPAs) usually have both positive effects of protection for the fisheries' target species and indirect negative effects for sea urchins. Moreover, often in MPAs sea urchin human harvest is restricted, but allowed. This study is aimed at estimating the effect of human harvest of the sea urchin Paracentrotus lividus within MPAs, where fish exploitation is restricted and its density is already controlled by a higher natural predation risk. The prediction we formulated was that the lowest densities of commercial sea urchins would be found where human harvest is allowed and where the harvest is restricted, compared to where the harvest is forbidden. Methods: At this aim, a collaborative database gained across five MPAs in Sardinia (Western Mediterranean, Italy) and areas outside was gathered collecting sea urchin abundance and size data in a total of 106 sites at different degrees of sea urchin exploitation: no, restricted and unrestricted harvest sites (NH, RH and UH, respectively). Furthermore, as estimates made in past monitoring efforts (since 2005) were available for 75 of the sampled sites, for each of the different levels of exploitation, the rate of variation in the total sea urchin density was also estimated. Results: Results have highlighted that the lowest sea urchin total and commercial density was found in RH sites, likely for the cumulative effects of human harvest and natural predation. The overall rate of change in sea urchin density over time indicates that only NH conditions promoted the increase of sea urchin abundance and that current local management of the MPAs has driven towards an important regression of populations, by allowing the harvest. Overall, results suggest that complex mechanisms, including synergistic effects between natural biotic interactions and human pressures, may occur on sea urchin populations and the assessment of MPA effects on P. lividus populations would be crucial to guide management decisions on regulating harvest permits. Overall, the need to ban sea urchin harvest in the MPAs to avoid extreme reductions is encouraged, as inside the MPAs sea urchin populations are likely under natural predation pressures for the trophic upgrading.

Trait gradients inform predictions of seagrass meadows changes to future warming.

Comparing populations across temperature gradients can inform how global warming will impact the structure and function of ecosystems. Shoot density, morphometry and productivity of the seagrass Posidonia oceanica to temperature variation was quantified at eight locations in Sardinia (western Mediterranean Sea) along a natural sea surface temperature (SST) gradient. The locations are spanned for a narrow range of latitude (1.5°), allowing the minimization of the effect of eventual photoperiod variability. Mean SST predicted P. oceanica meadow structure, with increased temperature correlated with higher shoot density, but lower leaf and rhizome width, and rhizome biomass. Chlorophyll a (Chl-a) strongly impacted seagrass traits independent of SST. Disentangling the effects of SST and Chl-a on seagrass meadow shoot density revealed that they work independently, but in the same direction with potential synergism. Space-for-time substitution predicts that global warming will trigger denser seagrass meadows with slender shoots, fewer leaves, and strongly impact seagrass ecosystem. Future investigations should evaluate if global warming will erode the ecosystem services provided by seagrass meadows.

Influence of foraging context on the whistle structure of the common bottlenose dolphin.

Sounds are particularly important for animals that live in complex social communities. In this study, we assessed the communication calls (whistles) that common bottlenose dolphins emit during their foraging activities in the absence and presence of motor boats and during dolphin depredation on trawlers, in Alghero (Sardinia, Italy) and Cres-Losinj Archipelago (Croatia). The latter behaviour involves foraging on concentrated food sources during very noisy human activity and may require the emission of distinctive whistles. Thus, we investigated if whistle structure, in terms of frequency and time parameters, changes depending on these three foraging contexts. In Sardinia, during foraging in interaction with trawlers, whistles differed from those emitted during the other foraging contexts. Conversely, in Cres-Losinj, significant variations in whistles were found to be related mainly to the presence of motor boats. This study represents the first report on how two dolphin populations adopt different acoustic tactics in the context of similar foraging behaviour. By investigating the effects of opportunistic foraging on acoustic repertoires, we provide new findings on the acoustic adaptation of dolphins to local conditions and contribute to understanding the relationships between dolphins and human activities, such as fishing and boat traffic.