Coralligenous reefs state along anthropized coasts: Application and validation of the COARSE index,based on a rapid visual assessment (RVA) approach

A rapid visual assessment (RVA) approach for the characterization and assessment of the integrity of coralligenous reefs was applied in 21 stations subjected to different levels of anthropogenic pressure, along the French Mediterranean coasts. The reefs were characterized from both the geomorphologic and bionomic (biotic cover, conspicuous species richness, canopy-forming species, etc.) points of view, and their health status was estimated through the COARSE (COralligenous Assessment by ReefScape Estimate) index. The sensitivity of the COARSE index and the robustness of the RVA approach to observer biases were analyzed. Results showed that most coralligenous reefs were characterized by (sub) vertical cliffs or platforms with variable slope, usually dominated by biotic facies with Paramuricea clavata and/or Eunicella cavolini in healthy stations, or by algal associations or facies of impoverishment in the most impacted situations. The overall quality scores of the COARSE index generally reflected the putative level of stress of the sampling stations; differences due to observer biases resulted negligible. Coupling the RVA approach with the COARSE index proved an effective protocol for both the characterization and the evaluation of coralligenous reefs: the former is achieved by the analysis of the whole complexity of this habitat, the latter provides for the first time an indication of sea-floor integrity, differently from previous indices that aim at estimating water quality.     

High Meiofaunal and Nematodes Diversity around Mesophotic Coral Oases in the Mediterranean Sea

Although the mesophotic zone of the Mediterranean Sea has been poorly investigated, there is an increasing awareness about its ecological importance for its biodiversity, as fish nursery and for the recruitment of shallow water species. Along with coastal rocky cliffs, isolated coralligenous concretions emerging from muddy bottoms are typical structures of the Mediterranean Sea mesophotic zone. Coralligenous concretions at mesophotic depths in the South Tyrrhenian Sea were investigated to assess the role of these coralligenous oases in relation to the biodiversity of surrounding soft sediments. We show here that the complex structures of the coralligenous concretions at ca. 110 m depth influence the trophic conditions, the biodiversity and assemblage composition in the surrounding sediments even at considerable distances. Coral concretions not only represent deep oases of coral biodiversity but they also promote a higher biodiversity of the fauna inhabiting the surrounding soft sediments. Using the biodiversity of nematodes as a proxy of the total benthic biodiversity, a high turnover biodiversity within a 200 m distance from the coralligenous concretions was observed. Such turnover is even more evident when only rare taxa are considered and seems related to specific trophic conditions, which are influenced by the presence of the coralligenous structures. The presence of a high topographic complexity and the trophic enrichment make these habitats highly biodiverse, nowadays endangered by human activities (such as exploitation of commercial species such as Corallium rubrum, or trawling fisheries, which directly causes habitat destruction or indirectly causes modification in the sedimentation and re-suspension rates). We stress that the protection of the coralligenous sea concretions is a priority for future conservation policies at the scale of large marine ecosystems and that a complete census of these mesophotic oases of biodiversity should be a priority for future investigations in the Mediterranean Sea.     

Into the depth of population genetics: pattern of structuring in mesophotic red coral populations

Deep-sea reef-building corals are among the most conspicuous invertebrates inhabiting the hard-bottom habitats worldwide and are particularly susceptible to human threats. The precious red coral (Corallium rubrum, L. 1758) has a wide bathymetric distribution, from shallow up to 800 m depth, and represents a key species in the Mediterranean mesophotic reefs. Several studies have investigated genetic variability in shallow-water red coral populations, while geographic patterns in mesophotic habitats are largely unknown. This study investigated genetic variability of C. rubrum populations dwelling between 55 and 120 m depth, from the Ligurian to the Ionian Sea along about 1500 km of coastline. A total of 18 deep rocky banks were sampled. Colonies were analyzed by means of a set of microsatellite loci and the putative control region of the mitochondrial DNA. Collected data were compared with previous studies. Both types of molecular markers showed high genetic similarity between populations within the northern (Ligurian Sea and Tuscan Archipelago) and the southern (Tyrrhenian and Ionian seas) study areas. Variability in habitat features between the sampling sites did not affect the genetic variability of the populations. Conversely, the patchy distribution of suitable habitats affected populations’ connectivity within and among deep coral banks. Based on these results and due to the emphasis on red coral protection in the Mediterranean Sea by international institutions, red coral could be promoted as a ‘focal species’ to develop management plans for the conservation of deep coralligenous reefs, a reservoir of marine biodiversity.     

Diversity of Porifera in the Mediterranean coralligenous accretions,with description of a new species

Temperate reefs, built by multilayers of encrusting algae accumulated during hundreds to thousands of years, represent one of the most important habitats of the Mediterranean Sea. These bioconstructions are known as “coralligenous” and their spatial complexity allows the formation of heterogeneous microhabitats offering opportunities for a large number of small cryptic species hardly ever considered.Although sponges are the dominant animal taxon in the coralligenous rims with both insinuating and perforating species, this group is until now poorly known. Aim of this work is to develop a reference baseline about the taxonomic knowledge of sponges and, considering their high level of phenotypic plasticity, evaluate the importance of coralligenous accretions as a pocket for biodiversity conservation.Collecting samples in four sites along the coast of the Ligurian Sea, we recorded 133 sponge taxa (115 of them identified at species level and 18 at genus level). One species, Eurypon gracilis is new for science; three species, Paratimea oxeata, Clathria (Microciona) haplotoxa and Eurypon denisae are new records for the Italian sponge fauna, eleven species are new findings for the Ligurian Sea. Moreover, seventeen species have not been recorded before from the coralligenous community. The obtained data, together with an extensive review of the existing literature, increase to 273 the number of sponge species associated with the coralligenous concretions and confirm that this habitat is an extraordinary reservoir of biodiversity still largely unexplored, not only taxonomically, but also as to peculiar adaptations and life histories.     

An integrative systematic approach to species diversity and distribution in the genus Mesophyllum (Corallinales,Rhodophyta) in Atlantic and Mediterranean Europe

For the first time, a comprehensive assessment of Mesophyllum species diversity and their distribution in Atlantic Europe and the Mediterranean Sea is presented based on molecular (COI-5P, psbA) and morphological data. The distribution ranges were redefined for the four species collected in this study: M. alternans, M. expansum, M. macroblastum and M. sphaericum. Mesophyllum sphaericum, which was previously known only from a single maerl bed in Galicia (NW Spain), is reported from the Mediterranean Sea. The known range of M. expansum (Mediterranean and Macaronesia) was extended to the Atlantic Iberian Peninsula. The occurrence of M. alternans was confirmed along the Atlantic French coast south to Algarve (southern Portugal). Mesophyllum lichenoides was only recorded from the Atlantic, whereas M. macroblastum appears to be restricted to the Mediterranean Sea. A positive correlation was observed between maximum Sea Surface Temperature (SSTmax) and the depth at which M. expansum was collected, suggesting that this species may compensate for higher SST by growing in deeper habitats where the temperature is lower. The latter indicates that geographic shifts in the distribution of coastal species as a result of global warming can possibly be mitigated by changes in the depth profile at which these species occur. Mesophyllum expansum, an important builder of Mediterranean coralligenous habitats, may be a good target species to assess its response to climate change.     

Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation

The structure, distribution, and temporal changes of epibenthic assemblages of a Mediterranean coralligenous reef were investigated using a multifactorial sampling design. The distribution of taxa on vertical walls and down-facing surfaces of overhangs and crevices was analysed at ten sites along 2 km of rocky reefs, south of Livorno (Ligurian Sea, Italy). The temporal variations were analysed between two periods (1995–1996 and 1997–1998) and among four sampling times within each period. Most of the space was dominated by prostrate seaweeds (including Peyssonnelia rubra, P. rosa-marina, and Mesophyllum lichenoides), turf-forming seaweeds, and the red coral Corallium rubrum. The cover of a variety of other invertebrates, mainly sponges and bryozoans, was less than 2%. All taxa were found on both vertical and down-facing surfaces. However, seaweeds dominated the vertical surfaces (mean cover >97%), while C. rubrum and other invertebrates dominated down-facing surfaces (mean density of C. rubrum >16 colonies dm⁻²). Although there was some fluctuation in the abundance of taxa, no obvious patterns were observed. These results support the model of limited temporal variability in Mediterranean coralligenous reefs, possibly related to the slow growth rates of the most abundant taxa and the reduced seasonality of physical conditions.     

Coralligenous “atolls”: Discovery of a new morphotype in the Western Mediterranean Sea

Coralligenous habitat and rhodoliths beds are very important in terms of biodiversity in the Mediterranean Sea. During an oceanographic campaign, carried out in northern Cap Corse, new coralligenous structures have been discovered. These structures, never previously identified in the Mediterranean Sea, are named “coralligenous atolls” because of their circular shape. The origin and growth dynamics of these atolls are still unknown but their form does not appear to result from hydrodynamic action and an anthropogenic origin also seems unlikely. However, this kind of shape seems rather closer to that of other circular structures (e.g. pockmarks) the origin of which is related to gaseous emissions. Further studies are needed to confirm this hypothesis through chemical analysis.     

Ecoregion-Based Conservation Planning in the Mediterranean: Dealing with Large-Scale Heterogeneity

Spatial priorities for the conservation of three key Mediterranean habitats, i.e. seagrass Posidonia oceanica meadows, coralligenous formations, and marine caves, were determined through a systematic planning approach. Available information on the distribution of these habitats across the entire Mediterranean Sea was compiled to produce basin-scale distribution maps. Conservation targets for each habitat type were set according to European Union guidelines. Surrogates were used to estimate the spatial variation of opportunity cost for commercial, non-commercial fishing, and aquaculture. Marxan conservation planning software was used to evaluate the comparative utility of two planning scenarios: (a) a whole-basin scenario, referring to selection of priority areas across the whole Mediterranean Sea, and (b) an ecoregional scenario, in which priority areas were selected within eight predefined ecoregions. Although both scenarios required approximately the same total area to be protected in order to achieve conservation targets, the opportunity cost differed between them. The whole-basin scenario yielded a lower opportunity cost, but the Alboran Sea ecoregion was not represented and priority areas were predominantly located in the Ionian, Aegean, and Adriatic Seas. In comparison, the ecoregional scenario resulted in a higher representation of ecoregions and a more even distribution of priority areas, albeit with a higher opportunity cost. We suggest that planning at the ecoregional level ensures better representativeness of the selected conservation features and adequate protection of species, functional, and genetic diversity across the basin. While there are several initiatives that identify priority areas in the Mediterranean Sea, our approach is novel as it combines three issues: (a) it is based on the distribution of habitats and not species, which was rarely the case in previous efforts, (b) it considers spatial variability of cost throughout this socioeconomically heterogeneous basin, and (c) it adopts ecoregions as the most appropriate level for large-scale planning.     

Mapping biodiversity in three-dimensions challenges marine conservation strategies: The example of coralligenous assemblages in North-Western Mediterranean Sea

Multi-facet diversity indices have been increasingly widely used in conservation ecology but congruence analyses both on horizontal and vertical axes have not yet been explored. We investigated the vertical and horizontal distributions of α and β taxonomic (TD), functional (FD) and phylogenetic diversity (PD) in a three-dimensional structured ecosystem. We focused on the Mediterranean coralligenous assemblages which form complex structures both vertically and horizontally, and are considered as the most diverse and threatened communities of the Mediterranean Sea. Although comparable to tropical reef assemblages in terms of richness, biomass and production, coralligenous assemblages are less known and more rarely studied, in particular because of their location in deep waters. Our study covers the entire range of distribution of coralligenous habitats along the French Mediterranean coasts, representing the most complete database so far developed for this important ecosystem. To our knowledge, this is the first analysis of spatial diversity patterns of marine biodiversity on both horizontal and vertical scales.Our study revealed that taxonomic diversity differed from functional and phylogenetic diversity patterns at the station level, the latter two being strongly structured by depth, with shallower stations generally richer than deeper ones. Considering all stations, phylogenetic diversity was less congruent to taxonomic diversity (Pearson's correlation of r = 0.48) but more congruent to functional diversity (r = 0.69) than randomly expected. Similar congruence patterns were revealed for stations deeper than 50 m (r = 0.44 and r = 0.84, respectively) but no significantly different congruence level than randomly expected was revealed among diversity facets for more shallow stations. Mean functional α- and β-diversity were lower than phylogenetic diversity and even lower than taxonomic α- and β-diversity for both vertical and horizontal scales. Low FD and PD values at both α- and β-diversity indicated functional and phylogenetic clustering. Community dissimilarities (β-diversity) increased over depth especially in central and eastern part of the French Mediterranean littoral and in northern Corsica, indicating coralligenous vertical structure within these regions. Overall horizontal β-diversity was higher within the 50–70 m depth belts.We conclude that taxonomic diversity alone is inadequate as a basis for setting conservation goals for this ecosystem and additional information, at least on phylogenetic diversity, is needed to preserve the ecosystem functioning and coralligenous evolutionary history. Our results highlight the necessity of considering different depth belts as a basis for regional scale conservation efforts. Current conservation approaches, such as the existing marine protected areas, are insufficient in preserving coralligenous habitats. The use of multi-facet indices should be considered, focusing on preserving local diversity patterns and compositional dissimilarities, both vertically and horizontally.     

Mediterranean Lithophyllum stictiforme (Corallinales,Rhodophyta) is a genetically diverse species complex: implications for species circumscription,biogeography and conservation of coralligenous habitats

Lithophyllum species in the Mediterranean Sea function as algal bioconstructors, contributing to the formation of biogenic habitats such as coralligenous concretions. In such habitats, thalli of Lithophyllum, consisting of crusts or lamellae with entire or lobed margins, have been variously referred to as either one species, L. stictiforme, or two species, L. stictiforme and L. cabiochiae, in the recent literature. We investigated species diversity and phylogenetic relationships in these algae by sequencing three markers (psbA and rbcL genes, cox2,3 spacer), in conjunction with methods for algorithmic delimitation of species (ABGD and GMYC). Mediterranean subtidal Lithophyllum belong to a well‐supported lineage, hereby called the L. stictiforme complex, which also includes two species described from the Atlantic, L. lobatum and L. searlesii. Our results indicate that the L. stictiforme complex consists of at least 13 species. Among the Mediterranean species, some are widely distributed and span most of the western and central Mediterranean, whereas others appear to be restricted to specific localities. These patterns are interpreted as possibly resulting from allopatric speciation events that took place during the Messinian Salinity Crisis and subsequent glacial periods. A partial rbcL sequence from the lectotype of L. stictiforme unambiguously indicates that this name applies to the most common subtidal Lithophyllum in the central Mediterranean. We agree with recent treatments that considered L. cabiochiae and L. stictiforme conspecific. The diversity of Lithophyllum in Mediterranean coralligenous habitats has been substantially underestimated, and future work on these and other Mediterranean corallines should use identifications based on DNA sequences.     

Modeling and predicting potential spawning habitat of anchovy (Engraulis encrasicolus) and round sardinella (Sardinella aurita) based on satellite environmental information

Anchovy and round sardinella are two important small pelagic species in the Mediterranean that spawn during the summer period. This is a first attempt to model and predict the two species’ potential spawning habitats in this area. Generalized additive models (GAMs) were constructed based on satellite environmental variables and presence/absence egg data, available from ichthyoplankton surveys conducted in the North Aegean Sea during early summer (June 2003–2006). These models were subsequently used to predict the probability of anchovy and round sardinella spawning in the Greek Seas as well as the entire Mediterranean and Black Sea during the same month of the year. The interaction of bottom depth and chlorophyll explained most of the deviance in the presence/absence GAMs of both species, indicating spawning over continental shelf areas with increased surface chlorophyll values. Round sardinella spawned closer to coast than anchovy. Predicted potential spawning areas for anchovy and round sardinella in unsampled areas of the Greek Seas and the entire Mediterranean and Black Sea were in good agreement with existing information on the distribution and extent of the spawning grounds, especially for anchovy. Modeling the species’ reproductive activity in relation to easily accessible environmental information and applying the models in a predictive way could be an initial, low-cost step to designate potential spawning fish habitats. Guest editor: V. D. Valavanis Essential Fish Habitat Mapping in the Mediterranean     

Aspetti Della Biocenosi Coralligena in Due Stazioni Dei Bacini Occidentale Ed Orientale Del Mediterraneo

Abstract

Facies of the coralligenous biocoenose in two stations of the Western and Eastern Mediterranean Basins. — The benthic comunities of circalittoral region have been studied by diving technique in the Western and Eastern Mediterranean Basins. The facies of the coralligenous biocoenose which show a larger difference between the two Basins are: 1) the communities of non calcareous algae in biotopes with constant direction depth streams and 2) the precoralligenous facies. These communities in the Aegean Sea are characterized by Sargassum linifolium, Cystoseira corniculata v. laxior, Caulerpa prolifera, Udotea petiolata, Dasycladus clavaeformis and by sponge Calix nicaeensis; in the Thyrrenean Sea by Laminaria rodriguezii, Cystoseira spinosa, Neurocaulon grandiflorum, Fauchea repens, Halymenia dichotoma, Callymenia reniformis and by the sponge Axinella cannabina. The environmental factors which determine these different facies in the circalittoral region of the two Mediterranean Basins are chiefly the temperature, the light intensity and the sedimentary rhythm.     

Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of mediterranean coralligenous outcrops

Increasing anthropogenic pressures urge enhanced knowledge and understanding of the current state of marine biodiversity. This baseline information is pivotal to explore present trends, detect future modifications and propose adequate management actions for marine ecosystems. Coralligenous outcrops are a highly diverse and structurally complex deep-water habitat faced with major threats in the Mediterranean Sea. Despite its ecological, aesthetic and economic value, coralligenous biodiversity patterns are still poorly understood. There is currently no single sampling method that has been demonstrated to be sufficiently representative to ensure adequate community assessment and monitoring in this habitat. Therefore, we propose a rapid non-destructive protocol for biodiversity assessment and monitoring of coralligenous outcrops providing good estimates of its structure and species composition, based on photographic sampling and the determination of presence/absence of macrobenthic species. We used an extensive photographic survey, covering several spatial scales (100s of m to 100s of km) within the NW Mediterranean and including 2 different coralligenous assemblages: Paramuricea clavata (PCA) and Corallium rubrum assemblage (CRA). This approach allowed us to determine the minimal sampling area for each assemblage (5000 cm(2) for PCA and 2500 cm(2) for CRA). In addition, we conclude that 3 replicates provide an optimal sampling effort in order to maximize the species number and to assess the main biodiversity patterns of studied assemblages in variability studies requiring replicates. We contend that the proposed sampling approach provides a valuable tool for management and conservation planning, monitoring and research programs focused on coralligenous outcrops, potentially also applicable in other benthic ecosystems.     

Coralligène formations in the eastern Mediterranean Sea: Morphology, distribution, mapping and relation to fisheries in the southern Aegean Sea (Greece) based on high-resolution acoustics

Coralline algae are one of the most important constructors of biogenic habitats. In the Mediterranean Sea, the dominant coralline algae species form crusts comprising formations known as coralligène, considered as very important fishing grounds by fishermen. Due to the destructive effect of fishing gear activities over coralligène, these formations were recently protected from the use of active benthic gears by the EU 1967/2006 Mediterranean fisheries management Regulation. However, the lack of maps and information on their distribution makes the effective application of these measures impossible. The present publication contributes to the mapping of coralligène in the southern Aegean Sea (eastern Mediterranean), and to the study of coralline algae formation morphology, distribution, development conditions and relation to fisheries using a combination of single-beam echo sounder, sidescan sonar, sub-bottom profiler recordings and biological and sedimentological ground-truthing techniques. The coralligène formations were recognized as two distinct acoustic signatures of localized backscatter facies distinguishable from other hard substrate reflectors at depths ranging from 55.9 to 114.0 m, but mainly between 70 and 90 m. Two types of formations were identified: minute reefs 0.5-2.5 m in height and superficial layer formations no more than 0.2 m thick over the substrate. The seismic profiles revealed a cavernous internal structure of the minute reefs and recorded their development on both hard and soft substrates. The distribution of formations was contagious, creating aggregations. The finding of superficial layer formations and coralline shreds around minute coralligène reefs indicated that the former could be an intermediate development type between isolated small coralline pebbles, rhodoliths, and minute reefs. Regarding the development conditions, sidescan sonar imagery indicated that the optimal conditions for the establishment and development of coralligène formations are medium intensity currents. Concerning human activity over coralligène, trawl traces were recorded near but not over minute reefs and both near and crossing superficial layer type aggregations, while a submarine cable was also recorded among minute reefs. The mapping of coralligène aggregation areas is essential for the application of the EU Regulation and the protection of this important marine habitat.     

Biodiversity and habitat mapping of Menorca Channel (western Mediterranean): implications for conservation

Menorca Channel (Balearic Islands, western Mediterranean) comprises 98,700 Ha of continental shelf. It has been proposed to include this area in the Natura 2000 network due to the wide range of species and habitats of high conservation value found here, such as Posidonia oceanica meadows and maërl and coralligenous beds. This study aimed to establish a scientific basis for managing and protecting the continental shelf bottoms in Menorca Channel. Sampling was carried out with side-scan sonar, beam trawls, box corers, a remote-operated vehicle and an underwater drop camera. The information collected was used to map the habitat distribution between 50 and 100 m depth, as well as make an inventory and describe the spatial patterns of both the specific and functional diversity. A total of 636 species was recorded in a mosaic of habitats in which Corallinacea calcareous algae and other soft red algae (Osmundaria volubilis and Peyssonnelia spp.) were the most abundant groups. Hotspots of specific and functional diversity were located in areas with high habitat heterogeneity and complexity. Protection of Menorca Channel should not only include the habitats and species in the European directives, but also the habitats that are not currently protected, such as O. volubilis and Peyssonnelia beds, due to their biogeographical and ecological interest and their contribution to the biodiversity of shelf bottoms in the Mediterranean Sea.     

Halocynthia papillosa (Linnaeus, 1767) as an indicator of SCUBA diving impact

The solitary ascidian Halocynthia papillosa (Linnaeus, 1767) is proposed as a good indicator of the deleterious effect of SCUBA diving on the Mediterranean coralligenous communities. A comparative survey of H. papillosa populations at frequented and unfrequented localities was carried out over a two-year period (during 2006 and 2007), before and after a peak diving season in the Sierra Helada Marine Park (SW Western Mediterranean Sea). We observed bigger and more abundant individuals of H. papillosa at undived sites than at frequented dived sites during the period of study. Furthermore, individuals of H. papillosa in the most frequented localities occupied more cryptic positions than in the undived localities. H. papillosa was shown to be very sensitive to the adverse effects of SCUBA diving. This species could represent a reliable bioindicator of diving activity and as such constitute a useful tool for the quick and easy monitoring of impact on coralligenous communities before this damage becomes unmitigatable.     

They are here to stay: the biology and ecology of lionfish (Pterois miles) in the Mediterranean Sea

The lionfish, Pterois miles, is one of the most recent Lessepsian immigrants into the Mediterranean Sea, and it poses a serious threat to marine ecosystems in the region. This study assesses the basic biology and ecology of lionfish in the Mediterranean, examining morphometrics, reproduction and diet as well as population structure and distribution. The population density of lionfish has increased dramatically in Cyprus since the first sighting in late 2012; by 2018 aggregations of up to 70 lionfish were found on rocky grounds with complex reefs and artificial reefs in depths of 0–50 m. Lionfish in Cyprus become mature within a year, and adults are capable of spawning year-round, with peak spawning in summer when the sea-surface temperature reaches 28.4°C. The Cypriot lionfish grow faster and bigger than in their native range, and females are more common than males. Lionfish are generalist predators in these waters, as also found in their native range, consuming a range of teleost and crustacean prey, some of which are of high economic value (e.g., Spicara smaris and Sparisoma cretense) or have an important role in local trophic webs (e.g., Chromis chromis). Overall, the reproductive patterns, the presence of juveniles and adults throughout the year, the rapid growth rates and the generalist diet indicate that lionfish are thriving and are now already well established in the region and could potentially become the serious nuisance that they are in their temperate and tropical western Atlantic–invasive range.