Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): biodiversity, distribution and vulnerability

Knowledge about deep-sea megabenthic communities has greatly increased during the last two decades thanks to the improvement of technical diving equipment, submersibles, remotely operated and autonomous vehicles. In the last 10 years, several studies, targeting the Mediterranean deep continental shelf or mesophotic zone (40-200 m), have reported the occurrence of rich hotspots of biodiversity, namely marine animal forests, dominated by habitat-forming species such as corals and sponges thriving in dim light conditions. This bathymetric range hosts the deepest extension of shallow-water animal forests as well as proper mesophotic assemblages thriving on the so-called roche du large ecosystems. These complex aggregations play a fundamental ecological role in the marine ecosystems (refuge effect, nursery area, benthic-pelagic coupling, biogeochemical cycles) and the characterization of their diversity and distribution is considered of primary interest worldwide. Explorations have depicted not only the diversity of these forests but also their vulnerability towards mechanical impacts inflicted by demersal fishing activities, especially in the overexploited Mediterranean basin. This leads to an urgent need to quantify the damages burdening on these sensitive ecosystems and to develop easy-to-apply tools to evaluate and monitor their environmental status, in order to provide effective conservation measures. This thesis aims to address these topics focusing on the marine animal forests of the Ligurian deep continental shelf. The Ligurian Sea represents one of the most studied Mediterranean basins due to several extensive researches, which have characterized the benthic and pelagic fauna mainly through SCUBA diving (shallow waters) and trawl surveys (bathyal waters) since the beginning of the last century. On the other hand, a large knowledge gap still exists for this region regarding the deep circalittoral megabenthic communities and, overall, on the anthropic threats insisting on deep-sea communities. Indeed, considering the significant amount of professional and recreational fishermen operating at these depths in the Ligurian region, it was crucial to carry out an extensive investigation in this area. In the present study, about 80 sites have been investigated during a four-years ROV survey conducted along the Ligurian deep continental shelf representing the most comprehensive study so far for the Italian waters. ROV footage was used to characterize the benthic biocoenoses thriving on soft and hard bottoms, determine the most relevant environmental factors driving their spatial distribution, and quantify the anthropogenic disturbance. Twelve major assemblages have been identified by means of community analysis, including gorgonian and hydrozoan forests, dense keratose sponge grounds, a Dendrophyllia cornigera facies, bryozoan beds and soft-bottom meadows of sabellids and alcyonaceans, some of them reported for the first time. Forests of black corals and Paramuricea macrospina aggregations have also been reported from the video footage, although with a more scattered distribution. The distribution of these assemblages is determined by different environmental parameters, namely depth, substrate type and inclination. The abundance of marine litter herein observed is among the highest ever recorded in Europe, with maximum values up to 7900 items ha-1. Abandoned, lost or discarded fishing gears represent the 81% of the total sightings, with the highest abundance recorded on the deep rocky shoals facing the largest fishing harbors and fleets. The majority of the fishing gears observed is attributable to artisanal and recreational fishing activities, suggesting that these represent the main source of litter in the Ligurian Sea. Urban litter, mainly represented by plastic, has also been observed, generally with higher abundances nearby large cities and river mouths. A multidisciplinary approach based on ROV explorations, background fishermen interviews and on-board bycatch monitoring has also been applied to obtain quantitative data on the impact of different fishing methods adopted within two Ligurian case studies. The study areas have been selected following a bathymetric point of view to study two different deep-sea ecosystems (a deep circalittoral coralligenous shoal exploited by a small-scale fishery and a trawling ground located nearby a cold-water coral thanatocoenoses), and the investigated parameters were designed to fulfil the criteria proposed by FAO for the identification of Vulnerable Marine Ecosystems (VMEs). A fine characterisation of the megabenthic assemblages and the fishing effort was obtained, as well as the quantification of no-target catches rates (with particular attention to structuring megabenthic invertebrates and rare species), and the frequency of gear entanglement and loss. This information allowed to initiate the process to delineate Fisheries Restricted Areas (FRAs), over these sensitive deep areas. Finally, to evaluate the environmental status of megabenthic assemblages thriving on mesophotic coralligenous or rocky reefs at temperate latitudes, a multiparametric index (MACS) integrating all possible sources of ROV-based information regarding community structure and impacts has been developed and validated. This practical tool was thought to have a large-scale application within the on-going Marine Strategy monitoring programs of these ecosystems. In conclusion, a georeferenced database of the location of diversity hotspots and sites of litter accumulation has been created, in order to set the baseline for the monitoring of Ligurian mesophotic sensitive animal forests. This dataset will provide managers and stakeholders the scientific information and the tools for the creation of an extensive network of deep-sea marine protected areas in the Ligurian basin

The cold-water coral province of the eastern Ligurian Sea (NW Mediterranean Sea): historical and novel evidences

Several bathyal cold-water coral provinces, characterized by a lush growth of habitat-forming scleractinians, have been recognized in the Mediterranean Sea. However, the search for this biogenic habitat only marginally targeted the Italian coast of the Ligurian Sea (NW Mediterranean basin) despite historical and a few recent local studies in the region reporting the presence of corals. This study used bathymetry maps, side-scan sonar profiles, historical charts, and trawling routes to identify sites that could potentially host coral habitats in the eastern sector of the Ligurian Sea. Remotely operated vehicle video footage from various projects (2015-2021, 20 dives) was then used to characterize four sub-areas (Genoa Plateau, Portofino, Deiva Marina, and Monterosso) where corals were detected between 450 m and 750 m depth. Radiocarbon dating was used to trace back the geological history of the coral structures. A small coral mound, impacted by trawling activities, was found on the Genoa Plateau, while four massive coral structures were found in the other sub-areas, mainly located in a morphologically complex and highly energetic canyon region. High levels of megafaunal biodiversity, including rarely reported alcyonaceans as Placogorgia coronata, were observed together with moderate fishing impact. Overall, the identified coral areas potentially account for 9 km(2) of both subfossil mounds (as old as 13300 years BP), dominated by Desmophyllum pertusum, and living reefs, dominated by Madrepora oculata, the latter representing up to 23% of the substrate coverage. The few living colonies of D. pertusum in the area represent the first documented records for the Ligurian Sea. These data support the presence of a distinct eastern Ligurian cold-water coral province

Brachiopod Fauna from the Deep Mediterranean Sea: Distribution Patterns and Ecological Preferences

Compared to their fossil counterparts, living brachiopods are investigated far less often, due to their occurrence in remote environments such as dark caves or deep environments. Due to the scarcity of studies targeting in situ brachiopods' populations, large-scale information on their distribution and ecological preferences is still lacking, especially on hardgrounds. The extensive employment of remotely operated vehicles (ROVs), however, has opened up the chance to better explore this taxon's diversity and ecology in the mesophotic and bathyal zones. The analysis of over 600 h of video footage collected from 624 sites, from 40 m to 1825 m, located along the Ligurian and Tyrrhenian coasts of Italy and the Sicily Channel, allowed for a large-scale investigation. The four identified species, Novocrania anomala, Gryphus vitreus, Megerlia truncata and Terebratulina retusa, emerged as common macrofaunal components of the explored habitats, especially between 150 m and 250 m, with high occurrences in the northern areas, especially on offshore seamounts. All species can form dense aggregations of individuals, with M. truncata showing the densest populations on steep rocky terraces (up to 773 individuals m(-2)). Except for G. vitreus, the only species also recorded on soft bottoms, the others were found exclusively on hardgrounds, with N. anomala showing a peculiar ability to exploit anthropogenic substrates such as terracotta amphorae. No stable species-specific associations were noted, even if numerous species were frequently observed together. Although brachiopods do not show the conspicuous tridimensionality of large filter-feeders, their substrate occupancy and their role in pelagic-benthic processes support their importance in deep-sea Mediterranean ecosystems

Facies created by the yellow coral Dendrophyllia cornigera (Lamarck, 1816): Origin, substrate preferences and habitat complexity

The yellow coral Dendrophyllia cornigera (Lamarck, 1816) is a NE Atlantic-Mediterranean scleractinian. It is considered a typical hard bottom species, generally reported on outcropping rocks from mesophotic to upper bathyal depths. Several evidences suggest that this species is able to tolerate a broad range of temperatures, which allows it to colonize numerous environments in a wide depth range. In the present study, we first provided a detailed ecological characterization of the D. cornigera dense aggregation thriving on the Mantice Shoal (NW Ligurian Sea, Mediterranean Sea). Information on substrate type and inclination, average extension and density, colonies size-class frequency distribution and associated fauna are reported. Then, we presented an extensive review of the available information on the ecology of this species, including 142 new ROV records from the Italian coast (40–1820 m). Results indicated that D. cornigera occurs on a wide range of substrates, including soft bottoms and hardgrounds (outcropping rocks, coralligenous rock and dead cold-water coral frameworks), with significant differences in colony density and size among different substrates. Dendrophyllia cornigera creates three main facies, each characterized by a specific combination of substrate, inclination, depth, and associated fauna. Scattered living colonies, as well as large thanatocoenoses, display a wide geographical and bathymetric distribution. Differently, the facies represented by dense meadows on horizontal soft-bottoms results rare, being reported only from the Mantice Shoal and the Amendolara Bank (Ionian Sea). The radiocarbon age of the thanatocoenoses varies between 400 (Corsica Channel) and 13000 (Vercelli Seamount) years before present. This study highlights the wide adaptability of D. cornigera in terms of environmental settings, changing the current view on the ecology of this species and providing essential insights for the implementation of international deep-sea habitat classification schemes and conservation measures

. Ecological role and phylogenetic position of a new habitat-forming species (Canalipalpata, Sabellidae) from the Mediterranean mesophotic soft-bottoms

This study presents a description of Bispira riccardi sp. nov., a new habitat-forming sabellid polychaete from the mesophotic NW Mediterranean Sea. Individuals, up to 20 cm long, show a peculiar morphology of radioles, thoracic uncini, companion chaetae and ventral shield of the collar. The phylogenetic position of this new taxon in the genus Bispira has been validated using nuclear (18S rRNA) and mitochondrial (COI) markers. Aggregations of B. riccardi sp. nov. were found by ROV on horizontal muddy bottoms between 56 and 85 m, in areas subjected to high trophic inputs. Patches are fragmented and dense (up to 943 individuals m 2) probably accounting for various hectares. A 5-days continuous monitoring, carried out using an autonomous lander, revealed that the contraction of the branchial crown was positively affected by temperature and current, rapidly responding to meteorological events. The filtering activity and high density of these fields suggest a considerable impact on the pelagic-benthic coupling and the amount of organic matter in the sediments. Indeed, meiofaunal abundance and diversity within the aggregations resulted significantly higher than in outer stations. These findings highlight the undisclosed potential of the deep Mediterranean Sea for sabellid diversity and their importance as habitat-forming species on mesophotic soft bottoms

Mediterranean bioconstructions along the Italian coast

Marine bioconstructions are biodiversity-rich, three-dimensional biogenic structures, regulating key ecological functions of benthic ecosystems worldwide. Tropical coral reefs are outstanding for their beauty, diversity and complexity, but analogous types of bioconstructions are also present in temperate seas. The main bioconstructions in the Mediterranean Sea are represented by coralligenous formations, vermetid reefs, deep-sea cold-water corals, Lithophyllum byssoides trottoirs, coral banks formed by the shallow-water corals Cladocora caespitosa or Astroides calycularis, and sabellariid or serpulid worm reefs. Bioconstructions change the morphological and chemicophysical features of primary substrates and create new habitats for a large variety of organisms, playing pivotal roles in ecosystem functioning. In spite of their importance, Mediterranean bioconstructions have not received the same attention that tropical coral reefs have, and the knowledge of their biology, ecology and distribution is still fragmentary. All existing data about the spatial distribution of Italian bioconstructions have been collected, together with information about their growth patterns, dynamics and connectivity. The degradation of these habitats as a consequence of anthropogenic pressures (pollution, organic enrichment, fishery, coastal development, direct physical disturbance), climate change and the spread of invasive species was also investigated. The study of bioconstructions requires a holistic approach leading to a better understanding of their ecology and the application of more insightful management and conservation measures at basin scale, within ecologically coherent units based on connectivity: the cells of ecosystem functioning

Effects of the 2018 exceptional storm on the Paramuricea clavata (Anthozoa, Octocorallia) population of the Portofino Promontory (Mediterranean Sea)

Exceptional meteo-marine events, such as storms, may have profound effects on the structure of benthic communities, yet their consequences on these ecosystems in the Mediterranean basin are still poorly known, mainly due to the unpredictability of such phenomena as well as the general lack of comparative datasets. The highly destructive storm of fall 2018, sustained by SE winds exceeding 130 kmh 121 and generating 10-m high waves, hit the coasts of the Ligurian Sea with devastating strength, producing vast damages and profound changes to the coastal morphology. Quantitative surveys performed soon after the catastrophic event were used to study the effects of the storm on the population structure of the habitat-forming gorgonian Paramuricea clavata (Risso, 1826) along the cliffs of the Portofino Promontory, a site particularly stricken by the storm. The same population was studied in 1997, 2002 and 2016, therefore it was possible to compare its health status before and after the impact of the storm. The P. clavata forest lost about one-third of the colonies between 2016 and 2018; colonies up to 25 m depth utterly disappeared, while below 30 m the storm effects were reduced, although the remaining population showed increased levels of epibiosis and necrosis. Over 21-years of observation, the effects of the storm have significantly slowed-down the recovery of the Portofino Promontory population after the massive mortality events of the last decades. Natural stress factors, although unpredictable, are fundamental to put into perspective changes in the benthic communities over time

Filling a Gap: A Population of Eunicella verrucosa (Pallas, 1766) (Anthozoa, Alcyonacea) in the Tavolara-Punta Coda Cavallo Marine Protected Area (NE Sardinia, Italy)

Among Mediterranean habitat-forming alcyonaceans, the sea fan Eunicella verrucosa is known to form dense forests at circalittoral depths, providing seascape complexity and sustaining a rich associated fauna. Its occurrence in the Tavolara–Punta Coda Cavallo Marine Protected Area (NE Sardinia) has never been deeply investigated despite this area being well known from a biocoenotic point of view. This study provides new information on the size of the colonies settled between 35 and 59 m depth on granitic outcrops and represents a contribution to highlighting the hotspot of megabenthic diversity enclosed in the protected area. The presence of 100 colonies was assessed by photographic samplings performed between 2015 and 2020, in a small area characterized by peculiar ecological conditions. The morphometric descriptions and age estimation showed a persistently isolated population probably derived from a stochastic event of settling of larvae presumably coming from the Tuscany Archipelago. A richly associated epibiotic community, composed of 18 species/OTUs, showed how branched bryozoans, particularly Turbicellepora avicularis, and the parasitic octocoral Alcyonium coralloides, affected the colonies’ branches, suggesting a putative anthropogenic impact related to fishing activity. This study indicates that proper protection and management strategies are mandatory for the Marine Protected Area, in order to conserve this unique population and the whole associated benthic assemblage

Filling a Gap: a population of Eunicella verrucosa (Pallas, 1766) (Anthozoa, Alcyonacea) in the Tavolara-Punta Coda Cavallo Marine Protected Area (NE Sardinia, Italy)

Among Mediterranean habitat-forming alcyonaceans, the sea fan Eunicella verrucosa is known to form dense forests at circalittoral depths, providing seascape complexity and sustaining a rich associated fauna. Its occurrence in the Tavolara–Punta Coda Cavallo Marine Protected Area (NE Sardinia) has never been deeply investigated despite this area being well known from a biocoenotic point of view. This study provides new information on the size of the colonies settled between 35 and 59 m depth on granitic outcrops and represents a contribution to highlighting the hotspot of megabenthic diversity enclosed in the protected area. The presence of 100 colonies was assessed by photographic samplings performed between 2015 and 2020, in a small area characterized by peculiar ecological conditions. The morphometric descriptions and age estimation showed a persistently isolated population probably derived from a stochastic event of settling of larvae presumably coming from the Tuscany Archipelago. A richly associated epibiotic community, composed of 18 species/ OTUs, showed how branched bryozoans, particularly Turbicellepora avicularis, and the parasitic octocoral Alcyonium coralloides, affected the colonies’ branches, suggesting a putative anthropogenic impact related to fishing activity. This study indicates that proper protection and management strategies are mandatory for the Marine Protected Area, in order to conserve this unique population and the whole associated benthic assemblage

Filling a Gap: A Population of <i>Eunicella verrucosa</i> (Pallas, 1766) (Anthozoa, Alcyonacea) in the Tavolara-Punta Coda Cavallo Marine Protected Area (NE Sardinia, Italy)

Among Mediterranean habitat-forming alcyonaceans, the sea fan Eunicella verrucosa is known to form dense forests at circalittoral depths, providing seascape complexity and sustaining a rich associated fauna. Its occurrence in the Tavolara–Punta Coda Cavallo Marine Protected Area (NE Sardinia) has never been deeply investigated despite this area being well known from a biocoenotic point of view. This study provides new information on the size of the colonies settled between 35 and 59 m depth on granitic outcrops and represents a contribution to highlighting the hotspot of megabenthic diversity enclosed in the protected area. The presence of 100 colonies was assessed by photographic samplings performed between 2015 and 2020, in a small area characterized by peculiar ecological conditions. The morphometric descriptions and age estimation showed a persistently isolated population probably derived from a stochastic event of settling of larvae presumably coming from the Tuscany Archipelago. A richly associated epibiotic community, composed of 18 species/OTUs, showed how branched bryozoans, particularly Turbicellepora avicularis, and the parasitic octocoral Alcyonium coralloides, affected the colonies’ branches, suggesting a putative anthropogenic impact related to fishing activity. This study indicates that proper protection and management strategies are mandatory for the Marine Protected Area, in order to conserve this unique population and the whole associated benthic assemblage