Role of macroalgal forests within Mediterranean shallow bays in blue carbon storage.

Although seaweeds rank among the most productive vegetated habitats globally, their inclusion within Blue Carbon frameworks is at its onset, partially because they usually grow in rocky substrates and their organic carbon (Corg) is mostly exported and stored beyond their habitat and thus, demonstrating its long-term storage is challenging. Here, we studied the sedimentary Corg storage in macroalgal forests dominated by Gongolaria barbata and in adjacent seagrass Cymodocea nodosa mixed with Caulerpa prolifera algae meadows, and bare sand habitats in Mediterranean shallow coastal embayments. We characterized the biogeochemistry of top 30 cm sedimentary deposits, including sediment grain-size, organic matter and Corg contents, Corg burial rates and the provenance of sedimentary Corg throughout stable carbon isotopes (δ13Corg) and pyrolysis analyses. Sediment Corg stocks and burial rates (since 1950) in G. barbata forests (mean ±â€¯SE, 3.5 ±â€¯0.2 kg Corg m-2 accumulated at 15.5 ±â€¯1.6 g Corg m-2 y-1) fall within the range of those reported for traditional Blue Carbon Ecosystems. Although the main species contributing to sedimentary Corg stocks in all vegetated habitats examined was C. nodosa (36 ±â€¯2 %), macroalgae contributed 49 % (19 ±â€¯2 % by G. barbata and 30 ±â€¯3 % by C. prolifera) based on isotope mixing model results. Analytical pyrolysis confirmed the presence of macroalgae-derived compounds in the sediments, including N-compounds and α-tocopherol linked to G. barbata and C. prolifera, respectively. The sedimentary Corg burial rate linked to macroalgae within the macroalgal forests examined ranged from 5.4 to 9.5 g Corg m-2 y-1 (7.4 ±â€¯2 g Corg m-2 y-1), which is 4-fold higher than previous global estimates. This study provides empirical evidence for the long-term (~70 years) sequestration of macroalgae-derived Corg within and beyond seaweed forests in Mediterranean shallow coastal embayments and thereby, supports the inclusion of macroalgae in Blue Carbon frameworks.

Capacity of countries to reduce biological invasions.

The extent and impacts of biological invasions on biodiversity are largely shaped by an array of socio-economic and environmental factors, which exhibit high variation among countries. Yet, a global analysis of how these factors vary across countries is currently lacking. Here, we investigate how five broad, country-specific socio-economic and environmental indices (Governance, Trade, Environmental Performance, Lifestyle and Education, Innovation) explain country-level (1) established alien species (EAS) richness of eight taxonomic groups, and (2) proactive or reactive capacity to prevent and manage biological invasions and their impacts. These indices underpin many aspects of the invasion process, including the introduction, establishment, spread and management of alien species. They are also general enough to enable a global comparison across countries, and are therefore essential for defining future scenarios for biological invasions. Models including Trade, Governance, Lifestyle and Education, or a combination of these, best explained EAS richness across taxonomic groups and national proactive or reactive capacity. Historical (1996 or averaged over 1996-2015) levels of Governance and Trade better explained both EAS richness and the capacity of countries to manage invasions than more recent (2015) levels, revealing a historical legacy with important implications for the future of biological invasions. Using Governance and Trade to define a two-dimensional socio-economic space in which the position of a country captures its capacity to address issues of biological invasions, we identified four main clusters of countries in 2015. Most countries had an increase in Trade over the past 25 years, but trajectories were more geographically heterogeneous for Governance. Declines in levels of Governance are concerning as they may be responsible for larger levels of invasions in the future. By identifying the factors influencing EAS richness and the regions most susceptible to changes in these factors, our results provide novel insights to integrate biological invasions into scenarios of biodiversity change to better inform decision-making for policy and the management of biological invasions. Supplementary Information: The online version contains supplementary material available at 10.1007/s11625-022-01166-3.

The challenge of setting restoration targets for macroalgal forests under climate changes.

The process of site selection and spatial planning has received scarce attention in the scientific literature dealing with marine restoration, suggesting the need to better address how spatial planning tools could guide restoration interventions. In this study, for the first time, the consequences of adopting different restoration targets and criteria on spatial restoration prioritization have been assessed at a regional scale, including the consideration of climate changes. We applied the decision-support tool Marxan, widely used in systematic conservation planning on Mediterranean macroalgal forests. The loss of this habitat has been largely documented, with limited evidences of natural recovery. Spatial priorities were identified under six planning scenarios, considering three main restoration targets to reflect the objectives of the EU Biodiversity Strategy for 2030. Results show that the number of suitable sites for restoration is very limited at basin scale, and targets are only achieved when the recovery of 10% of regressing and extinct macroalgal forests is planned. Increasing targets translates into including unsuitable areas for restoration in Marxan solutions, amplifying the risk of ineffective interventions. Our analysis supports macroalgal forests restoration and provides guiding principles and criteria to strengthen the effectiveness of restoration actions across habitats. The constraints in finding suitable areas for restoration are discussed, and recommendations to guide planning to support future restoration interventions are also included.

Learning takes time: Biotic resistance by native herbivores increases through the invasion process.

As invasive species spread, the ability of local communities to resist invasion depends on the strength of biotic interactions. Evolutionarily unused to the invader, native predators or herbivores may be initially wary of consuming newcomers, allowing them to proliferate. However, these relationships may be highly dynamic, and novel consumer-resource interactions could form as familiarity grows. Here, we explore the development of effective biotic resistance towards a highly invasive alga using multiple space-for-time approaches. We show that the principal native Mediterranean herbivore learns to consume the invader within less than a decade. At recently invaded sites, the herbivore actively avoided the alga, shifting to distinct preference and high consumptions at older sites. This rapid strengthening of the interaction contributed to the eventual collapse of the alga after an initial dominance. Therefore, our results stress the importance of conserving key native populations to allow communities to develop effective resistance mechanisms against invaders.

Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea.

Climate change is causing an increase in the frequency and intensity of marine heatwaves (MHWs) and mass mortality events (MMEs) of marine organisms are one of their main ecological impacts. Here, we show that during the 2015-2019 period, the Mediterranean Sea has experienced exceptional thermal conditions resulting in the onset of five consecutive years of widespread MMEs across the basin. These MMEs affected thousands of kilometers of coastline from the surface to 45 m, across a range of marine habitats and taxa (50 taxa across 8 phyla). Significant relationships were found between the incidence of MMEs and the heat exposure associated with MHWs observed both at the surface and across depths. Our findings reveal that the Mediterranean Sea is experiencing an acceleration of the ecological impacts of MHWs which poses an unprecedented threat to its ecosystems' health and functioning. Overall, we show that increasing the resolution of empirical observation is critical to enhancing our ability to more effectively understand and manage the consequences of climate change.

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.

Mediterranean rocky reefs in the Anthropocene: Present status and future concerns.

Global change is striking harder and faster in the Mediterranean Sea than elsewhere, where high levels of human pressure and proneness to climate change interact in modifying the structure and disrupting regulative mechanisms of marine ecosystems. Rocky reefs are particularly exposed to such environmental changes with ongoing trends of degradation being impressive. Due to the variety of habitat types and associated marine biodiversity, rocky reefs are critical for the functioning of marine ecosystems, and their decline could profoundly affect the provision of essential goods and services which human populations in coastal areas rely upon. Here, we provide an up-to-date overview of the status of rocky reefs, trends in human-driven changes undermining their integrity, and current and upcoming management and conservation strategies, attempting a projection on what could be the future of this essential component of Mediterranean marine ecosystems.

The role of competition and herbivory in biotic resistance against invaders: a synergistic effect.

Invasive species pose a major threat to global diversity, and once they are well established their eradication typically becomes unfeasible. However, certain natural mechanisms can increase the resistance of native communities to invaders and can be used to guide effective management policies. Both competition and herbivory have been identified as potential biotic resistance mechanisms that can limit plant invasiveness, but it is still under debate to what extent they might be effective against well-established invaders. Surprisingly, whereas biotic mechanisms are known to interact strongly, most studies to date have examined single biotic mechanisms separately, which likely influences our understanding of the strength and effectiveness of biotic resistance against invaders. Here we use long-term field data, benthic assemblage sampling, and exclusion experiments to assess the effect of native assemblage complexity and herbivory on the invasion dynamics of a successful invasive species, the alga Caulerpa cylindracea. A higher complexity of the native algal assemblage limited C. cylindracea invasion, probably through competition by canopy-forming and erect algae. Additionally, high herbivory pressure by the fish Sarpa salpa reduced C. cylindracea abundance by more than four times. However, long-term data of the invasion reflects that biotic resistance strength can vary across the invasion process and it is only where high assemblage complexity is concomitant with high herbivory pressure, that the most significant limitation is observed (synergistic effect). Overall, the findings reported in this study highlight that neglecting the interactions between biotic mechanisms during invasive processes and restricting the studied time scales may lead to underestimations of the true capacity of native assemblages to develop resistance to invaders.

Marine biomonitoring with eDNA: Can metabarcoding of water samples cut it as a tool for surveying benthic communities?

In the marine realm, biomonitoring using environmental DNA (eDNA) of benthic communities requires destructive direct sampling or the setting-up of settlement structures. Comparatively much less effort is required to sample the water column, which can be accessed remotely. In this study we assess the feasibility of obtaining information from the eukaryotic benthic communities by sampling the adjacent water layer. We studied two different rocky-substrate benthic communities with a technique based on quadrat sampling. We also took replicate water samples at four distances (0, 0.5, 1.5, and 20 m) from the benthic habitat. Using broad range primers to amplify a ca. 313 bp fragment of the cytochrome oxidase subunit I gene, we obtained a total of 3,543 molecular operational taxonomic units (MOTUs). The structure obtained in the two environments was markedly different, with Metazoa, Archaeplastida and Stramenopiles being the most diverse groups in benthic samples, and Hacrobia, Metazoa and Alveolata in the water. Only 265 MOTUs (7.5%) were shared between benthos and water samples and, of these, 180 (5.1%) were identified as benthic taxa that left their DNA in the water. Most of them were found immediately adjacent to the benthos, and their number decreased as we moved apart from the benthic habitat. It was concluded that water eDNA, even in the close vicinity of the benthos, was a poor proxy for the analysis of benthic structure, and that direct sampling methods are required for monitoring these complex communities via metabarcoding.

Differential effects of pollution on adult and recruits of a canopy-forming alga: implications for population viability under low pollutant levels.

Marine macroalgal forests are highly productive and iconic ecosystems, which are seriously threatened by number of factors such as habitat destruction, overgrazing, ocean warming, and pollution. The effect of chronic, but low levels of pollutants on the long-term survival of the canopy-forming algae is not well understood. Here we test the effects of low concentrations (found in good quality water-bodies) of nitrates, heavy metals copper (Cu) and lead (Pb), and herbicides (glyphosate) on both adults and recruits of Carpodesmia crinita, a Mediterranean canopy forming macroalga. We show that although adult biomass, height and photosynthetic yield remain almost unaffected in all the assays, low Cu levels of 30 µg/L completely suppress adult fertility. In addition, all the assays have a strong and negative impact on the survival and growth of recruits; in particular, glyphosate concentrations above 1 µg/L almost totally inhibit their survival. These results suggest that the long-term viability of C. crinita may be severely compromised by low pollutant levels that are not affecting adult specimens. Our results provide important data for a better understanding of the present-day threats to marine canopy-forming macroalgae and for the design of future management actions aimed at preserving macroalgal forests.

Management priorities for marine invasive species.

Managing invasive alien species is particularly challenging in the ocean mainly because marine ecosystems are highly connected across broad spatial scales. Eradication of marine invasive species has only been achieved when species were detected early, and management responded rapidly. Generalized approaches, transferable across marine regions, for prioritizing actions to control invasive populations are currently lacking. Here, expert knowledge was elicited to prioritize 11 management actions for controlling 12 model species, distinguished by differences in dispersion capacity, distribution in the area to be managed, and taxonomic identity. Each action was assessed using five criteria (effectiveness, feasibility, acceptability, impacts on native communities, and cost), which were combined in an 'applicability' metric. Raising public awareness and encouraging the commercial use of invasive species were highly prioritized, whereas biological control actions were considered the least applicable. Our findings can guide rapid decision-making on prioritizing management options for the control of invasive species especially at early stages of invasion, when reducing managers' response time is critical.

Biodiversity loss in a Mediterranean ecosystem due to an extreme warming event unveils the role of an engineering gorgonian species.

Stochastic perturbations can trigger major ecosystem shifts. Marine systems have been severely affected in recent years by mass mortality events related to positive thermal anomalies. Although the immediate effects in the species demography affected by mortality events are well known, information on the mid- to long-term effects at the community level is much less documented. Here, we show how an extreme warming event replaces a structurally complex habitat, dominated by long-lived species, by a simplified habitat (lower species diversity and richness) dominated by turf-forming species. On the basis of a study involving the experimental manipulation of the presence of the gorgonian Paramuricea clavata, we observed that its presence mitigated the effects of warming by maintaining the original assemblage dominated by macroinvertebrates and delaying the proliferation and spread of the invasive alga Caulerpa cylindracea. However, due to the increase of sediment and turf-forming species after the mortality event we hypothesize a further degradation of the whole assemblage as both factors decrease the recruitment of P.clavata, decrease the survival of encrusting coralligenous-dwelling macroinvertebrates and facilitate the spreading of C. cylindracea.

Response diversity in Mediterranean coralligenous assemblages facing climate change: Insights from a multispecific thermotolerance experiment.

Climate change threatens coastal benthic communities on a global scale. However, the potential effects of ongoing warming on mesophotic temperate reefs at the community level remain poorly understood. Investigating how different members of these communities will respond to the future expected environmental conditions is, therefore, key to anticipating their future trajectories and developing specific management and conservation strategies. Here, we examined the responses of some of the main components of the highly diverse Mediterranean coralligenous assemblages to thermal stress. We performed thermotolerance experiments with different temperature treatments (from 26 to 29°C) with 10 species from different phyla (three anthozoans, six sponges and one ascidian) and different structural roles. Overall, we observed species-specific contrasting responses to warming regardless of phyla or growth form. Moreover, the responses ranged from highly resistant species to sensitive species and were mostly in agreement with previous field observations from mass mortality events (MMEs) linked to Mediterranean marine heat waves. Our results unravel the diversity of responses to warming in coralligenous outcrops and suggest the presence of potential winners and losers in the face of climate change. Finally, this study highlights the importance of accounting for species-specific vulnerabilities and response diversity when forecasting the future trajectories of temperate benthic communities in a warming ocean.

The optimal sampling design for littoral habitats modelling: A case study from the north-western Mediterranean.

Species distribution models (SDMs) have been used to predict potential distributions of habitats and to model the effects of environmental changes. Despite their usefulness, currently there is no standardized sampling strategy that provides suitable and sufficiently representative predictive models for littoral marine benthic habitats. Here we aim to establish the best performing and most cost-effective sample design to predict the distribution of littoral habitats in unexplored areas. We also study how environmental variability, sample size, and habitat prevalence may influence the accuracy and performance of spatial predictions. For first time, a large database of littoral habitats (16,098 points over 562,895 km of coastline) is used to build up, evaluate, and validate logistic predictive models according to a variety of sampling strategies. A regularly interspaced strategy with a sample of 20% of the coastline provided the best compromise between usefulness (in terms of sampling cost and effort) and accuracy. However, model performance was strongly depen upon habitat characteristics. The proposed sampling strategy may help to predict the presence or absence of target species or habitats thus improving extensive cartographies, detect high biodiversity areas, and, lastly, develop (the best) environmental management plans, especially in littoral environments.

Under the canopy: Community-wide effects of invasive algae in Marine Protected Areas revealed by metabarcoding.

We analysed with multigene (18S and COI) metabarcoding the effects of the proliferation of invasive seaweeds on rocky littoral communities in two Spanish Marine Protected Areas. The invasive algae studied were Caulerpa cylindracea, Lophocladia lallemandii and Asparagopsis armata. They are canopy-forming, landscape-dominant seaweeds, and we were interested in their effects on the underlying communities of meiobenthos and macrobenthos, separated in two size fractions through sieving. A new semiquantitative treatment of metabarcoding data is introduced. The results for both markers showed that the presence of the invasive seaweed had a significant effect on the understory communities for Lophocladia lallemandii and Asparagopsis armata but not for Caulerpa cylindracea. Likewise, changes in MOTU richness and diversity with invasion status varied in magnitude and direction depending on the alga considered. Our results showed that metabarcoding allows monitoring of the less conspicuous, but not least important, effects of the presence of dominant invasive seaweeds.

Restoration of a Canopy-Forming Alga Based on Recruitment Enhancement: Methods and Long-Term Success Assessment.

Marine forests dominated by macroalgae have experienced noticeable regression along some temperate and subpolar rocky shores. Along continuously disturbed shores, where natural recovery is extremely difficult, these forests are often permanently replaced by less structured assemblages. Thus, implementation of an active restoration plan emerges as an option to ensure their conservation. To date, active transplantation of individuals from natural and healthy populations has been proposed as a prime vehicle for restoring habitat-forming species. However, given the threatened and critical conservation status of many populations, less invasive techniques are required. Some authors have experimentally explored the applicability of several non-destructive techniques based on recruitment enhancement for macroalgae restoration; however, these techniques have not been effectively applied to restore forest-forming fucoids. Here, for the first time, we successfully restored four populations of Cystoseira barbata (i.e., they established self-maintaining populations of roughly 25 m2) in areas from which they had completely disappeared at least 50 years ago using recruitment-enhancement techniques. We compared the feasibility and costs of active macroalgal restoration by means of in situ (wild-collected zygotes and recruits) and ex situ (provisioning of lab-cultured recruits) techniques. Mid/long-term monitoring of the restored and reference populations allowed us to define the best indicators of success for the different restoration phases. After 6 years, the densities and size structure distributions of the restored populations were similar and comparable to those of the natural reference populations. However, the costs of the in situ recruitment technique were considerably lower than those of the ex situ technique. The restoration method, monitoring and success indicators proposed here may have applicability for other macroalgal species, especially those that produce rapidly sinking zygotes. Recruitment enhancement should become an essential tool for preserving Cystoseira forests and their associated biodiversity.

An ecosystem-based approach to assess the status of Mediterranean algae-dominated shallow rocky reefs.

A conceptual model was constructed for the functioning the algae-dominated rocky reef ecosystem of the Mediterranean Sea. The Ecosystem-Based Quality Index (reef-EBQI) is based upon this model. This index meets the objectives of the EU Marine Strategy Framework Directive. It is based upon (i) the weighting of each compartment, according to its importance in the functioning of the ecosystem; (ii) biological parameters assessing the state of each compartment; (iii) the aggregation of these parameters, assessing the quality of the ecosystem functioning, for each site; (iv) and a Confidence Index measuring the reliability of the index, for each site. The reef-EBQI was used at 40 sites in the northwestern Mediterranean. It constitutes an efficient tool, because it is based upon a wide set of functional compartments, rather than upon just a few species; it is easy and inexpensive to implement, robust and not redundant with regard to already existing indices.

Structure and biodiversity of coralligenous assemblages dominated by the precious red coral Corallium rubrum over broad spatial scales.

Data on species diversity and structure in coralligenous outcrops dominated by Corallium rubrum are lacking. A hierarchical sampling including 3 localities and 9 sites covering more than 400 km of rocky coasts in NW Mediterranean, was designed to characterize the spatial variability of structure, composition and diversity of perennial species inhabiting coralligenous outcrops. We estimated species/taxa composition and abundance. Eight morpho-functional groups were defined according to their life span and growth to characterize the structural complexity of the outcrops. The species composition and structural complexity differed consistently across all spatial scales considered. The lowest and the highest variability were found among localities (separated by >200 km) and within sites (separated by 1-5 km), respectively supporting differences in diversity indices. The morpho-functional groups displayed a consistent spatial arrangement in terms of the number, size and shape of patches across study sites. These results contribute to filling the gap on the understanding of assemblage composition and structure and to build baselines to assess the response of this of this highly threatened habitat to anthropogenic disturbances.

Snapshot of a Bacterial Microbiome Shift during the Early Symptoms of a Massive Sponge Die-Off in the Western Mediterranean.

Ocean warming is affecting marine benthic ecosystems through mass mortality events that involve marine invertebrates, in particular bivalves, corals, and sponges. Among these events, extensive die-offs of Ircinia fasciculata sponges have been recurrently reported in western Mediterranean. The goal of our study was to test whether the temperature-related mass sponge die-offs were associated with or preceded by an early unbalanced bacterial microbiome in the sponge tissues. We took advantage of the early detection of disease and compared the microbiomes of healthy vs. early diseased I. fasciculata tissues. Our results showed a microbiome shift in early diseased tissues. The abundance of Gammaproteobacteria and Acidobacteria increased and that of Deltaproteobacteria decreased in diseased vs. healthy tissues. The change in community composition was also noticeable at the operational taxonomic unit (OTU) level. Diseased tissues contained more bacterial sequences previously identified in injured or stressed sponges and corals than healthy tissues. Bacterial diversity increased significantly in diseased tissues, which contained a higher number of low abundance OTUs. Our results do not support the hypothesis of one particular pathogen, whether a Vibrio or any other bacteria, triggering the Northwestern Mediterranean mass mortalities of I. fasciculata. Our data rather suggest an early disruption of the bacterial microbiome balance in healthy sponges through a shift in OTU abundances, and the purported consequent decline of the sponge fitness and resistance to infections. Opportunistic bacteria could colonize the sponge tissues, taking benefit of the sponge weakness, before one or more virulent pathogens might proliferate ending in the mass sponge die-off.

Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral.

In the current global climate change scenario, stressors overlap in space and time, and knowledge on the effects of their interaction is highly needed to understand and predict the response and resilience of organisms. Corals, among many other benthic organisms, are affected by an increasing number of global change-related stressors including warming and invasive species. In this study, the cumulative effects between warming and invasive algae were experimentally assessed on the temperate reef-builder coral Cladocora caespitosa. We first investigated the potential local adaptation to thermal stress in two distant populations subjected to contrasting thermal and necrosis histories. No significant differences were found between populations. Colonies from both populations suffered no necrosis after long-term exposure to temperatures up to 29 °C. Second, we tested the effects of the interaction of both warming and the presence of invasive algae. The combined exposure triggered critical synergistic effects on photosynthetic efficiency and tissue necrosis. At the end of the experiment, over 90% of the colonies subjected to warming and invasive algae showed signs of necrosis. The results are of particular concern when considering the predicted increase of extreme climatic events and the spread of invasive species in the Mediterranean and other seas in the future.