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.

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.

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.

The constraint of ignoring the subtidal water climatology in evaluating the changes of coralligenous reefs due to heating events.

Predicting community-level responses to seawater warming is a pressing goal of global change ecologists. How far such predictions can be derived from a fine gradient of thermal environments needs to be explored, even if ignoring water climatology does not allow estimating subtidal marine heat waves. In this study insights about the influence of the thermal environment on the coralligenous community structure were gained by considering sites (Sardinia, Italy) at different temperature conditions. Heating events were measured (by loggers at 18 m, 23 m, 28 m, 33 m and 38 m deep) and proxies for their duration (the maximum duration of events warmer than the 90th percentile temperature), intensity (the median temperature) and variability (the number of daily ΔT larger than the mean daily ΔT, and the number of heating events larger in ΔT than the 90th percentile ΔT) were selected by GAM models. Reliable predictions of decrease in coralligenous richness of taxa/morphological groups, with relevant increment in turfs and encrusting coralline algae abundance at the expenses of bryozoans were made. Associations to the different types of heating descriptor have highlighted the aspect (intensity, duration or variability) of the heating events and the threshold for each of them responsible for the trajectories of change.

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.

Concomitance of oligotrophy and low grazing pressure is essential for the resilience of Mediterranean subtidal forests.

The study aimed at investigating factors influencing the recovery of the canopy seaweed Cystoseira brachycarpa. A manipulative experiment was done to test if in barren patches the recovery of Cystoseira I) is enhanced by the removal of the urchins, II) is prevented by eutrophication, III) depends on the time of patch clearance and IV) decreases with the distance from Cystoseira bed edge within the barren patch. The effects of the same factors on the structure of the macroalgal assemblage were also tested. Cystoseira recovered abundantly only in clearings where nutrients were not added and urchins were removed. Furthermore, Cystoseira recovered irrespectively of the time the patches were cleared and the distance from the canopy edge. This study showed that the lack of sea urchins at oligotrophic conditions was essential for Cystoseira brachycarpa recruitment, providing evidence that interacting constraints are involved in the recovery of Cystoseira beds.

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.

The two facets of species sensitivity: Stress and disturbance on coralligenous assemblages in space and time.

Marine coastal ecosystems are affected by a vast array of human-induced disturbances and stresses, which are often capable of overwhelming the effects of natural changes. Despite the conceptual and practical difficulty in differentiating between disturbance and stress, which are often used interchangeably, the two terms bear different ecological meanings. Both are external agents, but the former causes mortality or physical damage (subtraction of biomass), whereas the latter causes physiological alteration (reduction in productivity). Sensitivity of marine organisms may thus have a dual connotation, being influenced in different ways by disturbance and by stress following major environmental change. Coralligenous assemblages, which shape unique biogenic formations in the Mediterranean Sea, are considered highly sensitive to change. In this paper, we propose a method to differentiate between disturbance and stress to assess the ecological status of the coralligenous assemblages. Disturbance sensitivity level (DSL) and stress sensitivity level (SSL) of the sessile organisms thriving in the coralligenous assemblages were combined into the integrated sensitivity level of coralligenous assemblages (ISLA) index. Changes in the coralligenous status were assessed in space, along a gradient of stress (human-induced pressures) at several sites of the western Mediterranean, and in time, from a long-term series (1961-2008) at Mesco Reef (Ligurian Sea) that encompasses a mass mortality event in the 1990s. The quality of the coralligenous assemblages was lower in highly urbanised sites than that in sites in both marine protected areas and areas with low levels of urbanisation; moreover, the quality of the assemblages at Mesco Reef decreased during the last 50years. Reduction in quality was mainly due to the increase in stress-tolerant and/or opportunist species (e.g. algal turfs, hydroids and encrusting sponges), the disappearance of the most sensitive macroalgae (e.g. Udoteaceae and erect Rhodophyta) and macro-invertebrates (e.g. Savalia savaglia, Alcyonium coralloides and Smittina cervicornis), and the appearance of invasive alien algal species. Although the specific indices of SSL or DSL well illustrated the changes in the spatial or temporal datasets, respectively, their integration in the ISLA index was more effective in measuring the change experienced by the coralligenous assemblages in both space and time.

The Seagrass Effect Turned Upside Down Changes the Prospective of Sea Urchin Survival and Landscape Implications.

Habitat structure plays an important mediating role in predator-prey interactions. However the effects are strongly dependent on regional predator pools, which can drive predation risk in habitats with very similar structure in opposite directions. In the Mediterranean Sea predation on juvenile sea urchins is commonly known to be regulated by seagrass structure. In this study we test whether the possibility for juvenile Paracentrotus lividus to be predated changes in relation to the fragmentation of the seagrass Posidonia oceanica (four habitat classes: continuous, low-fragmentation, high-fragmentation and rocks), and to the spatial arrangement of such habitat classes at a landscape scale. Sea urchin predation risk was measured in a 20-day field experiment on tethered individuals placed in three square areas 35×35 m2 in size. Variability of both landscape and habitat structural attributes was assessed at the sampling grain 5×5 m2. Predation risk changed among landscapes, as it was lower where more 'rocks', and thus less seagrass, were present. The higher risk was found in the 'continuous' P. oceanica rather than in the low-fragmentation, high-fragmentation and rock habitats (p-values = 0.0149, 0.00008, and 0.0001, respectively). Therefore, the expectation that juvenile P. lividus survival would have been higher in the 'continuous' seagrass habitat, which would have served as shelter from high fish predation pressure, was not met. Predation risk changed across habitats due to different success between attack types: benthic attacks (mostly from whelks) were overall much more effective than those due to fish activity, the former type being associated with the 'continuous' seagrass habitat. Fish predation on juvenile sea urchins on rocks and 'high-fragmentation' habitat was less likely than benthic predation in the 'continuous' seagrass, with the low seagrass patch complexity increasing benthic activity. Future research should be aimed at investigating, derived from the complex indirect interactions among species, how top-down control in marine reserves can modify seagrass habitat effects.

Limpets compensate sea urchin decline and enhance the stability of rocky subtidal barrens.

Understanding the mechanisms that regulate shifts among alternative ecosystems has become a priority for ecologists and environmental scientists. This study assessed the relative importance of different herbivorous invertebrates (urchins and limpets) in regulating transitions from barren to vegetated states on Mediterranean rocky reefs, under different levels of nutrient availability. Nutrient concentration and the herbivore assemblage were manipulated to test i) whether limpets can compensate for the decline or loss of sea urchin populations, thereby contributing to the persistence of barrens, ii) whether limpet effects vary according to nutrient availability and iii) whether limpets affect the structure of the algal assemblage. The complete removal of sea urchins was not sufficient to trigger the recovery of erect and turf-forming macroalgae if limpets were left at natural density, suggesting that these herbivores play an important role in the stability of the barren state. The effect of these mesograzers was particularly important under oligotrophic conditions. This suggests that limpets play an important role in sustaining the stability of the barren state. A more comprehensive assessment of top-down forces, implying the quantification of the relative effect of different herbivore guilds, is therefore necessary to estimate the strength of hysteresis and to identify critical thresholds at which shifts back to the vegetated state are initiated.

Suitability of the ALien Biotic IndEX (ALEX) for assessing invasion of macroalgae across different Mediterranean habitats.

The ALien Biotic IndEX (ALEX) has been recently proposed to evaluate biological invasions in soft-bottom macro-invertebrate assemblages. The present paper proposes the use of ALEX in sessile assemblages of Mediterranean hard bottom habitats and tests it along gradients of invasion. For five invasive macroalgae a variable number of case studies per each of four habitats were examined from the available data sets. For each case study samples were attributed to four levels of invasion depending on the abundance of the invading macroalgae. Results showed that the application of ALEX to sessile assemblages of hard bottoms allows to qualify the level of invasion along the considered gradients. Moreover, the decline of index values matched the impact of invasion on species number of the assemblages. Results also suggest that the concurrent use of ALEX and indices of benthic quality status can be a valuable tool to assess biopollution in hard bottom habitats.

Threats to macroalgal coralligenous assemblages in the Mediterranean Sea.

Coralligenous habitat is one of the most important coastal systems of the Mediterranean Sea. This paper evaluates the main threats to macroalgal coralligenous habitats through a review of the relevant literature. Sedimentation, nutrient enrichment and biological invasions can cause severe alterations in the structure of coralligenous assemblages due to the regression of perennial structuring species and increases in populations of ephemeral algae. Under pristine conditions, mechanical disturbance seems to be easily mitigated by the recovery capability of coralligenous assemblages; however, such disturbances seriously affect coralligenous structure if they occur in concert with other stressors. Important synergetic effects among all the studied anthropogenic disturbances are also highlighted. The main consequences of the considered stressors are the loss of the complexity of macroalgal assemblages and the deterioration of both alpha and beta diversity.

Effects of nutrient enrichment on macroalgal coralligenous assemblages.

Effects of eutrophication on marine ecosystems have been widely studied, even if both the effects on deep subtidal rocky assemblages and response of different successional stages to nutrients impact are still not clear. In this context, the study aimed to evaluate the effects of nutrient enrichment on Mediterranean macroalgal assemblages associated with coralligenous habitat. A manipulative field experiment was carried out by supplying both mature and early successional stages of assemblages with nutrients. A total of 62 macroalgal species were identified. Multivariate and univariate analyses showed that the structure of both mature and early successional macroalgal assemblages of coralligenous significantly varied between areas treated with nutrients and not treated areas. Moreover, differences were stronger when macroalgal assemblages were in the early successional stage than in the mature one. Results highlighted the role played by nutrients in determining the structure of macroalgal coralligenous assemblages, furthermore suggesting possible synergetic effects with other kinds of disturbances.

The spread of Caulerpa racemosa var. cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity.

The present study aims to evaluate if invasion of Caulerpa racemosa var. cylindracea can affect both alpha and beta diversity in Mediterranean coastal system. The following hypotheses were tested: (i) measures of alpha diversity differ between invaded and non-invaded assemblages (ii) this pattern is consistent between different habitats, (iii) assemblages from habitats which are naturally very different tend to be more similar when invaded compared to non-invaded situations. Results showed that Mediterranean benthic assemblages invaded by C. racemosa var. cylindracea were characterized by lower values of alpha diversity than non-invaded assemblages; moreover, differences between deep (25 m) and shallow water (5m) assemblages appeared lower in invaded than in non-invaded areas, with a decrease of beta diversity. This homogenisation of habitats was related to a lack of several characteristic species and to a higher abundance of few opportunistic species in invaded areas, particularly turf-forming algae. Moreover, variability in taxa composition was lower in invaded than in non-invaded assemblages in both habitats.

Sediment disturbance and loss of beta diversity on subtidal rocky reefs.

How changes in environmental complexity and heterogeneity affect beta diversity is poorly known. We investigated patterns of beta diversity in subtidal assemblages of algae and invertebrates in the northwest Mediterranean in relation to inclination of the substratum and sedimentation. Vertical and horizontal substrata supported distinct assemblages under low, but not under heavy, ambient loads of sediment. To test the hypothesis that sediment reduced the dissimilarity between assemblages, sedimentation was increased experimentally in plots established on vertical and horizontal surfaces at sites experiencing low ambient levels of sedimentation. Patterns were compared to those occurring at unmanipulated sites and at sites exposed to heavy loads of sediment about 2 km apart. After one year, assemblages on vertical substrata were indistinguishable from those occurring on flat surfaces at manipulated sites and both converged toward those occurring at sites exposed to heavy loads of sediment. Control sites still supported distinct assemblages on vertical and horizontal substrata by the end of the experiment. Similar effects of sediment were observed on recovering assemblages in experimental clearings. These results show that sediment increased similarity in assemblages overriding the influence of habitat complexity on beta diversity at small and large spatial scales.

Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposition.

This study tested whether the development of coralligenous assemblages on horizontal and vertical surfaces differed between localities of high and low sediment deposition. The development and structure of these assemblages varied in predictable ways according to the level of sediment deposition. These differences were largely independent of the orientation of substratum. Turfs were more extensive in areas of high sediment deposition while erect and encrusting algae were most extensive in areas of low sediment deposition. Encrusting invertebrates characterised vertical surfaces and were most extensive in areas of high sediment deposition. These results are consistent with studies from other temperate regions of the globe, suggesting that effects of sedimentation on temperate coasts are substantial and widespread.