**5. Discussion**

Macrobenthic invertebrates, such as soft and hard corals, contribute to the formation of heterogeneous and complex habitats on slopes, in canyons, and on seamounts, which constitute VMEs. Deep VMEs are hotspots of biodiversity, due to the variety of species they host, and are valuable fishing areas due to the occurrence of large individuals of commercial species and higher catches than in adjacent areas (e.g., [20,55,58,69,70]).

The deep-sea species distributed in the deep-sea habitats and VMEs of the Mediterranean make up 7% of the total quantified landings of approximately 788,000 tonnes [1]. The Ionian Sea is the basin where the largest fraction (about 40%) of the Mediterranean's deep resources is captured. This basin, in addition to being the deepest in the entire Mediterranean, presents an articulated and complex hydrography and geomorphology of the seabed, with canyons, banks, rocky bottoms, and VMEs where soft and hard coral species thrive (e.g., [81,92–94,142–144]).

Catches from official FAO statistics show consistency with catches from MEDITS trawl surveys. In both cases, abundance fluctuations were observed for most species. The most abundant deep-sea food resources in the Ionian Sea are the European hake (*M. merluccius*), the deep-water rose shrimp (*P. longirostris*), and the deep-water red shrimps (*A. foliacea* and *A. antennatus*). Other deep-sea food resources are represented by the crustacean *N. norvegicus*, the teleost fish *Lophius* spp., *C. conger*, *H. dactylopterus*, *P. bogaraveo*, *P. blennoides*, and *P. americanus*, and the shark *G. melastomus.*

For some species, significant increases in abundances have been observed, and this may be related to the reduction in fishing effort (e.g., *A. foliacea*, *P. longirostris*, *P. bogaraveo)*, the increase in SBT (e.g., *A. foliacea*, *P. longirostris*), and the presence of refuge areas scarcely accessible to fishing, which constitute VMEs and sites of resource renewal (e.g., *A. foliacea*, *H. dactylopterus*, *P. bogaraveo*, and, to a lesser extent, *P. blennoides* and *M. merluccius*). In particular, adult individuals of *P. bogaraveo* were almost exclusively collected in VMEs

between the southwestern Adriatic and northwestern Ionian seas (e.g., [71,78–80,145]). The golden shrimp (*P. martia*) was also found to be associated with the presence of corals [145].

Time-series data for the period 1985–2005 reveal a positive relationship of *A. foliacea* and *P. longirostris* abundances with a rise in the water temperature. Inverse relationships of *A. foliacea*, *P. longirostris*, *N. norvegicus*, and *P. blennoides* abundances with FE were also detected [78].

The increase in the abundance of *P. longirostris* observed in the northwestern Ionian Sea has also been reported in all European Mediterranean waters, demonstrating that the abundance of some stock is closely linked to climate change [146]. The increase in temperature observed in recent years may have produced an increase in suprabenthos, e.g., *Lophogaster typicus*, which represents the main prey of the deep-water rose shrimp [146,147]. In addition, as observed in the northern Tyrrhenian, high temperatures and low wind circulation negatively affect the recruitment of *M. merluccius.* Hake juveniles prey upon *P. longirostris* juveniles [148], so the lower predation pressure could have further enhanced the recruitment success of the shrimp [146,149]. The significant increase in abundance detected for *A. foliacea* is consistent with observations in the eastern Ionian Sea and southern Adriatic Sea [150]. However, for both *P. longirostris* and *A. foliacea*, the reduction in FE may have influenced the increase in their abundances.

Regarding *A. antennatus*, in the western Mediterranean it was observed that this deepwater shrimp seems to prefer relatively cold temperatures (13.1–13.2 ◦C) and relatively salty waters (>38.5) with low currents and moderate variability [123]). However, the occurrence of *A. antennatus* appears to be driven in a nonlinear manner by environmental conditions, including local temperature [123].

Times-series data regarding the abundance of *M. merluccius* in the northwestern Ionian for the period 1985–2005 reveal a positive relationship with the NAO index [78]. Recently, it has been observed that environmental factors can affect the spatiotemporal distribution pattern of the European hake throughout the Mediterranean basin [151]. In particular, high predicted biomass levels were observed especially at 200 m and between 14 and 18 ◦C, highlighting the preference of the species for colder waters. Moreover, the high biomass of this teleost fish has been correlated with the presence of nursery areas in many Mediterranean areas, some of which have been identified along the northwestern Ionian and in the southwestern Adriatic [152–155], connected to VMEs [81,83]. In this respect, the effect of the presence of the SML VME has been detected for *M. merluccius* and other deep-water species, in agreemen<sup>t</sup> with previous investigations in the central Mediterranean (e.g., [12,71,81,83,85,98]). Indeed, the SML CWC province has an effect on the abundance of deep-water resources, while also contributing to the spillover of individuals of commercial species exploited in the surrounding fishing grounds, subjected to a greater fishing pressure than in other areas of the northwestern Ionian Sea.

The most abundant species captured on the muddy bottoms, both by commercial fishing (FAO data) and during trawl surveys (MEDITS data), are also those most frequently caught in sensitive habitats and VMEs. Most of these species exhibit a bigger– deeper pattern, both on muddy bottoms—where larger individuals are generally caught by trawling—and in sensitive habitats and VMEs, partially protected from fishing due to the roughness of the seabed and the presence of rocks and hard corals. The largest individuals distributed in deep waters and in VMEs represent the adult fraction of the stocks. These are breeder individuals that often concentrate in VMEs, making them EFHs, since these ecosystems act as spawning and nursery areas [12,57,71,81,98], contributing to the renewal of the stocks on fishing grounds [83]. Both the spillover (i.e., active movement of juveniles and adults into fished areas) and larval seeding (i.e., the dispersal of eggs and larvae in fished areas) may contribute to the renewal of stocks in neighbouring fishing grounds. All of the species examined in this study carry out their life cycles on the bathyal bottoms by distributing themselves between muddy bottoms and refuge areas represented by VMEs, but only in these ecosystems is their vulnerability to fishing activities greatly reduced. In fact, models developed using data from trawl surveys carried out on muddy bottoms

provide indications of overfishing status for most of the species examined in the present study (e.g., [156]).

Species with a wide bathymetric distribution, such as anglers, have not shown any significant trend over time. Norway lobster, for both types of data, showed a decrease in abundance over time. This may be due to the fact that this species needs soft bottoms to dig burrows in the mud, which are also the most subjected to trawling. Another explanation deals with the negative relationship between Norway lobster biomass and SST, with the lowest indices associated with high temperatures [146]. The decreasing abundance related to higher temperatures is due to the reduction in the organic matter flux resulting from the decreased rainfall and river discharge, which influences benthic feeders and predators such as the Norway lobster [146,147].

Several deep-water species also represent an important feeding resource for several species of odontocetes inhabiting the offshore areas of the northwestern Ionian Sea [157–160]. Bathyal bentho-pelagic squids are fundamental prey of the Risso's dolphin (*Grampus griseus*) and the sperm whale (*Physeter macrocephalus*). Myctophids and demersal species, such as *M. merluccius*, are hunted by the striped dolphin (*Stenella coeruleoalba*) [161–164]. The trophic interactions between cetaceans and deep-water prey contribute to the recycling of energy and matter in the pelagic domain and coastal areas. Odontocetes can increase the CO2 absorption capability of phytoplankton, thus playing a critical role in climatic regulation [165]. Thus, the managemen<sup>t</sup> of deep sensitive habitats and their species contributes to ensuring the stability of several biological components that play a critical role in ecosystem functioning [164].

The increase in landings observed for Tunisia and Albania could be due to the fact that there are still deep areas that are largely unexploited by fishing activity. Moreover, here, the fishing pressure is lower than that along the Italian coasts of the central Mediterranean.

The VMEs are often impacted by commercial fishing (e.g., [17,20,64,68,69,82,98,103, 104,106,107,127,129]). An overview of available information on the incidental catch of VME indicator taxa from fishery-dependent and fishery-independent surveys has been recently provided by Chimienti et al. [55]. Bottom trawls represent the most impactful fishing practice to deep soft-bottom VMEs, followed by longlines, gillnets, pots, and traps.

Other human activities—including oil and gas exploration and exploitation, pollution, marine litter, ocean acidification, and climate change—are also harmful to VMEs and their biodiversity on the open slopes, canyons, and seamounts (e.g., [14,64,69,126,166–168]). In addition, biodiversity loss affects ecosystem services (ESs) and impairs the ocean's capacity to provide food, maintain water quality, and recover from disturbance [169–172]. ESs are the benefits that humans derive, either directly or indirectly, from the functions of ecosystems [173]. The Millennium Ecosystem Assessment (MA) [174] estimates that 60% of global ecosystem services are degraded or are being managed unsustainably. As biodiversity is lost and ecosystems are degraded, the biocapacity of the planet to support living organisms decreases. As biocapacity decreases, there are diminishing resources available to support a growing human population [175]. These considerations also concern the Mediterranean and its VMEs that provide several ESs [54] and, as noted above, many of them are in danger due to anthropogenic impacts.

The habitat structured by macrobenthic invertebrates in VMEs is a supporting ES that provides organisms—including those of commercial species—with suitable physical and chemical features, food and spatial resources, places for courtship, mating, and spawning, breeding sites and nurseries, places to hide from predators, and refuges to escape from adverse environmental conditions (e.g., [38,45,58,72,176,177]). The decline of the habitat can cause negative effects on the species that use it for bioecological processes, affecting community composition and ecosystem functioning [178,179].

A strategy based on ecosystem-based fishery managemen<sup>t</sup> (EBFM) was adopted by the EU Common Fishery Policy (CFP) for fishery management, with the overall objective of sustaining healthy marine ecosystems and the fisheries that they support [180]. This implies sustainable managemen<sup>t</sup> not only of the commercial stocks, but also of the whole

environmental system that supports their production, including the importance of the economic and social dimensions.

Worldwide, fish consumption has grown enormously since 1961, surpassing even that of several species of the most common terrestrial animals in the human diet. Thinking about the fact that food innovation and sustainability are mainly based on systems where it is produced and systems by which food is collected, there is an urgen<sup>t</sup> need to protect deep-sea habitats and VMEs by promoting the use of sustainable fishing systems.

Many governments have made international commitments to the conservation of marine biodiversity. In particular, since the adoption of the Convention on Biological Diversity (CBD) in 1992, biodiversity considerations in relation to the managemen<sup>t</sup> of fisheries and aquaculture have been focused on policies and actions for the conservation of threatened species and vulnerable habitats. Within the CBD context, the scientific criteria to identify ecologically and biologically significant marine areas have been established [181], with the aim of defining managemen<sup>t</sup> measures that ensure the conservation of the biodiversity of these areas. The process in the Mediterranean was started by a regional workshop in 2014 [182], and culminated at the CBD COP 12 with the endorsement of 15 ecologically and biologically significant marine areas, recognising the biological and ecological significance of deep-sea habitats in the Mediterranean [64]. Following specific UNGA resolutions [183–185], similar criteria were adopted by the FAO [46] to identify VMEs and to develop international guidelines for the managemen<sup>t</sup> of deep-sea fisheries in the high seas, in order to ensure the protection of certain groups of species and habitats from significant adverse impacts (SAIs) caused by fisheries.

The Habitats Directive (92/43/EEC) [186] considers the CWC biotope as the habitat type "1170 Reefs", for which measures should be taken to maintain and restore a conservation status for this type of habitat. As part of the Barcelona Convention, the protocol concerning the specially protected areas and biological diversity adopted in 1995 is a tool for implementing the CBD, since it aims to protect and conserve biodiversity in valuable areas and species in the Mediterranean Sea. More recently, the Marine Strategy Framework Directive [187] aims to ensure that the collective pressure of human activities on the environment is kept within levels compatible with the achievement of good environmental status. This can also be achieved through the creation of marine protected areas (MPAs) focused on achieving a balance between sustainable fisheries and other human activities and habitat conservation. Although several conservation initiatives have been developed with the aim of protecting threatened hotspots of marine biodiversity, the marine protected areas (MPAs) that have been designated in deep waters are very limited [64,188,189].

During the last few decades, the Mediterranean deep-sea habitats have been protected through the institution of fishery restricted areas (FRAs), established by the General Fishery Commission for the Mediterranean and Black Sea (GFCM) with the aim of protecting VMEs and/or essential fish habitats (EFHs). To date, 10 FRAs have been established by the GFCM, including 1 large deep-water FRA below 1000 m. Trawling is forbidden in areas deeper than 1000 m in depth throughout the Mediterranean Sea. However, this conservation measure is not enough, considering that most of the coral habitats known so far are present within this depth limit. For this reason, the limitation of trawling up to 800 m depth would be more effective for the conservation of deep-sea coral habitats [54,64]. The FRAs aim to protect EFHs and/or sensitive habitats of high ecological value, such as VMEs, from any SAIs of fishing activities [46]. In particular, only two of the existing FRAs in the Mediterranean Sea have been created to target the conservation of a CWC habitat—namely, the *Lophelia* Reef off Santa Maria di Leuca (Italy, Ionian Sea) [82] and, more recently, the Bari Canyon in the southern Adriatic Sea (recommendation GFCM/44/2021/3) [133]. Three FRAs in the Strait of Sicily (northeast and northwest Malta) and one in the Gulf of Lion include some CWC sites, but they have been created to manage fishing stocks; thus, trawling is present there, albeit somewhat regulated. The Jabuka/Pomo Pit FRA aims to protect EFHs and an unquantified sea pen field [190], while the Eratosthenes Seamount FRA targets the protection of peculiar geological formations (with only a few

specimens of solitary scleractinians recorded) [138], and the Nile Delta FRA is characterised by the presence of chemosynthetic fauna [54]. Trawling and dredging are forbidden in the FRAs for the conservation of VMEs, while they are regulated in those for the managemen<sup>t</sup> of EFHs. Bottom longlining can be allowed—often in a buffer zone and under authorisation—depending on the regulations of the single FRA, while artisanal fishing practices are usually not performed in offshore areas, such as in the existing FRAs. These FRAs are currently isolated, while a desirable network of FRAs is a long way from being created. This network should be established in the pathway of the Mediterranean water mass circulation in order to connect the different FRAs all over the basin by means of larval dispersal [53,83,129].

As part of goal 14 (life below water) of the 2030 Sustainable Development Agenda [191], all of the targets regard VMEs, and specifically targets 14.2 (protect and restore ecosystems), 14.3 (reduce ocean acidification), and 14.4 (sustainable fishing). More recently, the EU Biodiversity Strategy for 2030 [192] reports that biodiversity is also seen as essential for safeguarding EU and global food security; its loss threatens our food systems, putting our food security and nutrition at risk.

### **6. Conclusions and Recommendations**

In the EU, at least 30% of the land surface and 30% of the sea should be protected, and for areas with high value or potential for biodiversity and, therefore, greater vulnerability, more stringent protection is needed.

Regarding the deep-sea sensitive habitats and VMEs, the implementation of a network of protected or fishing-restricted areas represents a fundamental measure to guarantee the proper conservation of the sites known in the Mediterranean Sea. A network of protected areas (mostly MPAs and FRAs) would satisfy both the conservation of vulnerable habitats and the managemen<sup>t</sup> of fishery resources according to the EBFM [63]. In this respect, after the past and recent establishment of the FRAs in the SML CWC province and Bari Canyon, respectively, appropriate spatial measures aimed at preserving the ecological function of *I. elongata facies* identified in the southern Adriatic should be adopted [98]. The Bari Canyon, *I. elongata facies*, and SML CWC province are in the path of the flow of the dense-water masses that pour from the southern Adriatic into the northern Ionian [53,81,92,94,97,129,193]. This stream of water masses connects the deep-sea coral communities distributed along the Apulian margin, which represent a network of refuge/renewal areas of fishery resources [81] that needs coherent conservation measures and managemen<sup>t</sup> strategies according to the EBFM [53–55].

In the southern Adriatic, the activity of trawler fleets is more concentrated on the continental shelf and on the upper part of the slope, with target species including the European hake, red mullet, spottail mantis shrimp, deep-water rose shrimp, and Norway lobster [194]. This explains the persistence of *I. elongata* in the southern Adriatic [98], and would sugges<sup>t</sup> that the protection measure to be adopted would be accepted by the fishermen. If not accepting an area closure measure, other managemen<sup>t</sup> approaches—such as encounter protocols with associate thresholds—can be developed and implemented according to the FAO's International Guidelines for the Management of Deep-Sea Fisheries [46,195], in order to ensure the protection of *I. elongata* from SAIs. In addition, the use of onboard observers and the correct adoption of digital logbooks could be applicable to trawl fishing vessels, as well as to most of the deep-sea benthic longlining vessels, which must be equipped with vessel monitoring by satellite systems (VMSs) and/or automated identification systems (AISs). The managemen<sup>t</sup> and control of the many small artisanal fishing boats, which use gillnets and trammel nets in shallower waters, could be achieved through the designation of landing points, obligations of notice of arrival in port, and control of landings [54].

Through blue growth (BG), the European Union seeks to meet human needs—such as food and energy—in a sustainable way, by creating new jobs and new sources of growth while safeguarding biodiversity and protecting the marine environment, thus preserving the services that healthy and resilient marine and coastal ecosystems provide [196]. In

this respect, marine spatial planning [187] consists of a public process of analysing and allocating the spatial and temporal distribution of human activities in marine areas to achieve ecological, economic, and social objectives, reducing conflicts and creating synergies between different activities, while protecting the environment by assigning protected areas, calculating impacts on ecosystems, and identifying opportunities for multiple uses of space. The use of an ecosystem for economic returns and social benefits must be done in a way that minimises negative impacts. If an ecosystem is degraded, the ESs that are derived from it will also be modified, including those concerning the availability and safety of food.

The good governance of an ecosystem requires, first of all, knowledge and monitoring of its condition. The central Mediterranean is an area with a complex hydrology and geomorphology, rich in biodiversity and biological resources, requiring greater knowledge and continuous monitoring of sensitive habitats and VMEs, as well as their associated biotic components, which can represent food resources [64,76]. Danovaro et al. [197] used expert elicitation (1155 deep-sea scientists consulted and 112 respondents) to indicate a wide consensus that monitoring should prioritise large organisms (that is, macro- and megafauna) living in deep waters and in benthic habitats, whereas monitoring of ecosystem functioning should focus on trophic structure and biomass production. They suggested that deep-sea conservation efforts should focus primarily on VMEs and habitat-forming species.

This is of particular importance in relation to the growth of human populations and the expansion of activities regarding the deep-sea environment, and for which the involvement of stakeholders with an interest in the deep-sea will be necessary, together with mechanisms that promote wide participation at the national and international levels, and that ensure conservation and long-term effective ecosystem-based fishery managemen<sup>t</sup> measures.

**Author Contributions:** Conceptualisation: G.D. and P.M.; investigation: G.D., P.M., L.S., F.C., A.C., G.C., R.C., P.R. and A.T.; contributed materials/analyses/tables/figures: C.C., F.C., L.S., P.M. and P.R.; writing—original draft preparation: G.D. and P.M.; references: A.C.; corresponding author: F.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** The data used in this study were collected under the Data Collection Framework (DCF), supported by the Italian Ministry of Agriculture, Food and Forestry Policy (MiPAAF) and by the European Commission (EU Regulations 1004/2017).

**Institutional Review Board Statement:** All specimens analysed in this study were collected from the fishery (Data Collection Framework [DCF]; EU Reg. 199/2008). Therefore, this study does not comply with the European Commission recommendations (Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010) or with Italian National Law (Decree Law n. 26 of 4 March 2014) on the protection of animals used for scientific experiment.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** The data used in this study were collected under the Data Collection Framework (DCF), supported by the Italian Ministry of Agriculture, Food and Forestry Policy (MiPAAF) and by the European Commission (EU Regulations 1004/2017). Data provided are owned by the Italian Ministry of Agriculture, Food and Forestry Policy (MiPAAF).

**Acknowledgments:** The authors thank their colleague Richard Lusardi, a native English-speaking expert, for manuscript review and Daniela Potenza, graphics expert, for the editing of the Figures.

**Conflicts of Interest:** The authors declare no conflict of interest.
