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Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): Biodiversity, Distribution and Vulnerability

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Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): Biodiversity, Distribution and Vulnerability Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): biodiversity, distribution and vulnerability Francesco Enrichetti Genova 2019 PhD Thesis 1 2 Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): biodiversity, distribution and vulnerability Francesco Enrichetti Genova 2019 PhD Thesis 3 4 Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): biodiversity, distribution and vulnerability Francesco Enrichetti PhD program in Sciences and Technologies for the Environment and the Landscape (STAT) XXXI cycle in Marine Sciences (5824) May 2019 Supervisor: Co-supervisor: Dr. Marzia Bo Prof. Giorgio Bavestrello 5 6 “Mesophotic Animal Forests of the Ligurian Sea (NW Mediterranean Sea): biodiversity, distribution and vulnerability” (2019). External referees: Prof. Francesco Mastrototaro from the University of Bari and Dr. Andrea Gori from the University of Salento. Cover: Ligurian mesophotic animal forests with gorgonians (Eunicella verrucosa) and Spongia (Spongia) lamella. Photo by Simonepietro Canese (ISPRA). 7 8 Mais, pendant quelques minutes, je confondis involontairement les règnes entre eux, prenant des zoophytes pour des hydrophytes, des animaux pour des plantes. Et qui ne s’y fût pas trompé ? La faune et la flore se touchent de si près dans ce monde sous-marin ! […] « Curieuse anomalie, bizarre élément, a dit un spirituel naturaliste, où le règne animal fleurit, et où le règne végétal ne fleurit pas ! » Jules Verne, Vingt mille lieues sous les mers 9 10 Table of contents SUMMARY 15 RIASSUNTO 17 INTRODUCTION 19 1. Deep-sea scientific exploration 19 2. Mesophotic animal forests of the Mediterranean Sea 21 3. Mediterranean fisheries and fishing impact on mesophotic animal forests 24 4. Conservation of Mediterranean animal forests 28 5. Study area: the Ligurian Sea 32 6. General objectives of this thesis 34 References 36 PART 1 - BIODIVERSITY 45 Chapter 1 - Megabenthic assemblages of the Ligurian deep continental shelf (NW Mediterranean Sea) 47 1. Introduction 48 2. Material and Methods 50 3. Results 54 4. Discussion 66 References 74 Supplemental material 81 11 PART 2 - FISHING IMPACT 89 Chapter 2 - Artisanal fishing impact on deep coralligenous animal forests: a Mediterranean case study of marine vulnerability 91 1. Introduction 92 2. Material and Methods 93 3. Results 99 4. Discussion 108 5. Conclusions 112 References 113 Supplemental material 118 Chapter 3 - Placogorgia coronata frist documented record in Italian waters: Use of trawl bycatch to unveil vulnerable deep-sea ecosystems 123 1. Introduction 124 2. Material and Methods 125 3. Results 128 4. Discussion 136 Reference 142 PART 3 - MONITORING AND CONSERVATION 147 Chapter 4 - Marine litter assessment and distribution on the deep Ligurian continental shelf (NW Mediterranean Sea) 149 1. Introduction 150 2. Material and Methods 152 3. Results 157 4. Discussion 163 References 169 Supplemental material 173 12 Chapter 5 - Assessing the environmental status of temperate mesophotic reefs: a new, integrated methodological approach 177 1. Introduction 178 2. Material and Methods 179 3. Results 189 4. Discussion 194 References 197 Supplemental material 202 CONCLUSIONS 205 Part 1 - Biodiversity 205 Part 2 - Fishing impact 206 Part 3 - Monitoring and conservation 207 Future perspectives 208 ANNEXES 211 ACKNOWLEDGEMENTS 214 13 14 Summary Knowledge about deep-sea megabenthic easy-to-apply tools to evaluate and communities has greatly increased during monitor their environmental status, in the last two decades thanks to the order to provide effective conservation improvement of technical diving measures. This thesis aims to address equipment, submersibles, remotely these topics focusing on the marine operated and autonomous vehicles. In animal forests of the Ligurian deep the last 10 years, several studies, continental shelf. targeting the Mediterranean deep The Ligurian Sea represents one of the continental shelf or mesophotic zone (40- most studied Mediterranean basins due 200 m), have reported the occurrence of to several extensive researches, which rich hotspots of biodiversity, namely have characterized the benthic and marine animal forests, dominated by pelagic fauna mainly through SCUBA habitat-forming species such as corals diving (shallow waters) and trawl surveys and sponges thriving in dim light (bathyal waters) since the beginning of conditions. This bathymetric range hosts the last century. On the other hand, a the deepest extension of shallow-water large knowledge gap still exists for this animal forests as well as proper region regarding the deep circalittoral mesophotic assemblages thriving on the megabenthic communities and, overall, so-called roche du large ecosystems. on the anthropic threats insisting on These complex aggregations play a deep-sea communities. Indeed, fundamental ecological role in the marine considering the significant amount of ecosystems (refuge effect, nursery area, professional and recreational fishermen benthic-pelagic coupling, biogeochemical operating at these depths in the Ligurian cycles) and the characterization of their region, it was crucial to carry out an diversity and distribution is considered of extensive investigation in this area. primary interest worldwide. Explorations In the present study, about 80 sites have have depicted not only the diversity of been investigated during a four-years these forests but also their vulnerability ROV survey conducted along the Ligurian towards mechanical impacts inflicted by deep continental shelf representing the demersal fishing activities, especially in most comprehensive study so far for the the overexploited Mediterranean basin. Italian waters. ROV footage was used to This leads to an urgent need to quantify characterize the benthic biocoenoses the damages burdening on these thriving on soft and hard bottoms, sensitive ecosystems and to develop determine the most relevant 15 environmental factors driving their spatial different deep-sea ecosystems (a deep distribution, and quantify the circalittoral coralligenous shoal exploited anthropogenic disturbance. Twelve major by a small-scale fishery and a trawling assemblages have been identified by ground located nearby a cold-water coral means of community analysis, including thanatocoenoses), and the investigated gorgonian and hydrozoan forests, dense parameters were designed to fulfil the keratose sponge grounds, a criteria proposed by FAO for the Dendrophyllia cornigera facies, bryozoan identification of Vulnerable Marine beds and soft-bottom meadows of Ecosystems (VMEs). A fine sabellids and alcyonaceans, some of characterisation of the megabenthic them reported for the first time. Forests of assemblages and the fishing effort was black corals and Paramuricea obtained, as well as the quantification of macrospina aggregations have also been no-target catches rates (with particular reported from the video footage, although attention to structuring megabenthic with a more scattered distribution. The invertebrates and rare species), and the distribution of these assemblages is frequency of gear entanglement and loss. determined by different environmental This information allowed to initiate the parameters, namely depth, substrate type process to delineate Fisheries Restricted and inclination. Areas (FRAs), over these sensitive deep The abundance of marine litter herein areas. observed is among the highest ever Finally, to evaluate the environmental recorded in Europe, with maximum status of megabenthic assemblages values up to 7900 items ha-1. Abandoned, thriving on mesophotic coralligenous or lost or discarded fishing gears represent rocky reefs at temperate latitudes, a the 81% of the total sightings, with the multiparametric index (MACS) integrating highest abundance recorded on the deep all possible sources of ROV-based rocky shoals facing the largest fishing information regarding community harbors and fleets. The majority of the structure and impacts has been fishing gears observed is attributable to developed and validated. This practical artisanal and recreational fishing tool was thought to have a large-scale activities, suggesting that these represent application within the on-going Marine the main source of litter in the Ligurian Strategy monitoring programs of these Sea. Urban litter, mainly represented by ecosystems. plastic, has also been observed, In conclusion, a georeferenced database generally with higher abundances nearby of the location of diversity hotspots and large cities and river mouths. sites of litter accumulation has been A multidisciplinary approach based on created, in order to set the baseline for ROV explorations, background fishermen the monitoring of Ligurian mesophotic interviews and on-board bycatch sensitive animal forests. This dataset will monitoring has also been applied to provide managers and stakeholders the obtain quantitative data on the impact of scientific information and the tools for the different fishing methods adopted within creation of an extensive network of deep- two Ligurian case studies. The study sea marine protected areas in the areas have been selected following a Ligurian basin. bathymetric point of view to study two 16 Riassunto Grazie alle innovazioni tecnologiche nel stato di salute delle biocenosi campo della subacquea tecnica, dei mesofotiche, permettendo di delineare sommergibili e dei robot filoguidati (ROV) efficaci misure di conservazione. Questa e autonomi, la conoscenza sulle comunità tesi si propone di affrontare tali tematiche
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