**1. Introduction**

Seafood is a fundamental source of proteins and nutrients for human nutrition. Its global consumption has increased since 1960 at rates per year higher than that of all land animals, combined and individually (i.e., bovine, ovine, porcine, etc.), except for poultry [1]. However, with the increasing demand for sea products, most of the fishery resources of the world's oceans have been overfished, and many are in a condition of variable levels according to the vulnerability of the different species. In addition, the overfishing condition of continental shelf fish resources has pushed the fishing activities to move towards the exploitable living resources of the deep sea [2–4]. In this regard, deep waters (i.e., beyond the continental shelf, and deeper than approximately 200 m) have acted as a refuge for several stocks with an extensive vertical distribution, where no fishing was occurring until the first decades of the last century [5]. With the expansion of fishing to deeper waters, favoured by the development of new technologies, muddy deep bottoms and other deep-water refuges—such as soft-bottom coral gardens (CGs), cold-water coral (CWC) reefs, submarine canyons (SCs), and seamounts (SEs)—have been affected by this activity, and may no longer play their role of providing structure, food, and shelter for

**Citation:** Maiorano, P.; Capezzuto, F.; Carluccio, A.; Calculli, C.; Cipriano, G.; Carlucci, R.; Ricci, P.; Sion, L.; Tursi, A.; D'Onghia, G. Food from the Depths of the Mediterranean: The Role of Habitats, Changes in the Sea-Bottom Temperature and Fishing Pressure. *Foods* **2022**, *11*, 1420. https://doi.org/10.3390/ foods11101420

Received: 4 April 2022 Accepted: 9 May 2022 Published: 13 May 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

fishery resources. All of these deep-water ecosystems have been identified as hotspots of biodiversity (e.g., [6–8]), and since they can be valuable fishing sites, due to the occurrence of large sizes and high abundances of commercial species, they are often impacted by commercial fishing [9–20]. Fisheries for some deep-sea fish stocks have also collapsed due to heavy pressure on species whose life history traits do not make them well-suited to an intensive harvest [3,4,21]. In fact, deep-sea fish species have a longer lifespan, slow growth, and later sexual maturity, and are consequently more vulnerable and less resilient to overfishing [22–27].

The EU began to deal with deep-sea fisheries in 1992, as a result of assessments carried out by the International Council for the Exploration of the Sea (ICES), who stated that most of the deep-water species of commercial interest were overfished [28]. The current scientific evidence suggests that many deep-sea fish stocks are being exploited beyond sustainable levels [23,29–32], thus emphasising the need to improve the managemen<sup>t</sup> of these species [3,32–35].

It is well-known that fishing can impact harvested populations directly by excessive removal of individuals, and indirectly by reducing habitat complex structures that guarantee their bioecological activities and provide protection from predators, as well as from adverse physical factors (e.g., [36–40]). Globally, around 40% of trawling fishing grounds are on waters deeper than the continental shelf [41], and several deep-sea habitats and ecosystems have been impacted by fishery activities, with consequent depletion of or reduction in economically important species (e.g., [3,9,21,42–45]).

According to the FAO [46], vulnerable marine ecosystems (VMEs) are groups of species, communities, or habitats that may be vulnerable to impacts from fishing activities. Corals, together with sponges, echinoderms, molluscs, and other epibenthic species, play a significant role in the formation of VMEs. Furthermore, most coral taxa are included in relevant lists of protected species, such as the Red List drawn up by the International Union for the Conservation of Nature (IUCN) [47–50]. Their vulnerability is linked to their likelihood of experiencing substantial alterations from short-term or chronic disturbances, as well as to their difficulty in recovering (for example, slow growth rate, late age of maturity, low or unpredictable recruitment, and long life expectancy) [51–55]. In addition, there is sufficient evidence that VMEs act as essential fish habitats (EFHs), defined as "those waters and substrates necessary to fish for spawning, breeding, feeding, or growth to maturity" [56–58]. Therefore, there is an international consensus in favour of the protection of VMEs in order to combine conservation and fisheries-management objectives according to the ecosystem approach to fisheries (EAF) [46,59–64].

Fish consumption has always been an important part of people's diets around the Mediterranean Sea. The annual production of about 788,000 tonnes, for a total revenue of USD 3.4 billion, offers employment opportunities to several hundred thousand people, supplies seafood products for human consumption to local and regional markets, and creates many other indirect benefits, although fisheries and related activities also produce a large amount of marine litter (including plastics) as a global increasing threat [1]. In the Mediterranean Sea the exploitation of deep-water resources only started in the first decades of the last century. In particular, the deep-water red shrimps *Aristaeomorpha foliacea* (giant red shrimp) and *Aristeus antennatus* (blue and red shrimp) were the target species for deep-water bottom trawling in the 1930s in the Ligurian Sea, where catches of these two shrimps were between 100 and 200 kg/day and, after the Second World War, they could be up to 1000 kg/day per boat [65,66]. In the 1940s, these resources began to be exploited in the Catalan and Balearic seas, and subsequently in other Mediterranean areas [67]. In the Mediterranean Basin, the development of deep-water commercial fisheries was due to the narrowness of the shelf, crossed by several submarine canyons, as well as the growth of the human population along the basin and high demand for a muchappreciated food. However, considering the multispecies nature of the Mediterranean fisheries, the deep-water red shrimps are mostly caught in bathyal muddy bottoms, between 400 and 800 m, together with many other valuable demersal species, such as the European

hake (*Merluccius merluccius*), the deep-water rose shrimp (*Parapenaeus longirostris*), the Norway lobster (*Nephrops norvegicus*), the blackspot seabream (*Pagellus bogaraveo*), the greater forkbeard (*Phycis blennoides*), and the wreckfish (*Polyprion americanus*). Other deepwater species of commercial interest, such as the blue whiting (*Micromesistius poutassou*), European conger (*Conger conger*), blackbelly rosefish (*Helicolenus dactylopterus*), angler (*Lophius piscatorius*), blackbellied angler (*Lophius budegassa*), blackmouth catshark (*Galeus melastomus*), bluntnose sixgill shark (*Hexanchus griseus*), golden shrimp (*Plesionika martia*), southern shortfin squid (*Illex coindetii*), European flying squid (*Todarodes sagittatus*), and lesser flying squid (*Todaropsis eblanae*), represent additional components of deep catches. Most of the fish species are commonly caught with trawl nets, longlines, and gillnets, while crustaceans and cephalopods are fished mainly with trawl nets, and sometime with pots.

Most of the abovementioned species are distributed across a wide depth range, between shelf and slope; some of them are typically distributed in deep waters. Moreover, past and recent investigations in deep-sea habitats with a complex and heterogeneous structure—such as coral ecosystems, submarine canyons, and seamounts (now considered VMEs)—have proven that most of the abovementioned species use these types of habitats for shelter, feeding, spawning, and nursery (e.g., [20,58,68–71]). Indeed, habitat features play an important role in determining the structure of species assemblages, and habitat loss may impact—albeit in different ways—on all life stages and critical phases of the different species [38,72]. While adult individuals may not be strictly affected by habitat as juveniles, the detrimental effects of habitat loss on juvenile survival may have longer-term impacts on adult populations [73].

The innovation and sustainability of the food (in the present case, the fishery resources represented by deep-sea fish, crustaceans, and molluscs) used by humanity are mainly based on the systems where it is produced (i.e., the deep-sea sensitive habitats and VMEs), and on the systems that allow its harvest (i.e., the fishing techniques). As part of the "*Innovations in the Food System: Exploring the Future of Food*" Special Issue, this paper aims (1) to briefly review studies that highlight a link between deep-sea fishery resources and VMEs in the Mediterranean Sea; (2) to provide new insights into commercial and experimental catches of the deep-sea fishery resources in the central Mediterranean for the past 30 years; (3) to evaluate changes in the abundance of these resources with time, sea-bottom temperature (SBT), fishing effort (FE), and depth; and (4) to reveal an effect of the Santa Maria di Leuca cold-water coral province on the abundance of the deepsea fishery resources. The implications of these findings and the presence of several geomorphological features, sensitive habitats, and VMEs in the central Mediterranean are discussed in terms of conservation of biodiversity, combined with the sustainable managemen<sup>t</sup> of the fishery resources.

### **2. Materials and Methods**

Data on food resources from deep-sea sensitive habitats and VMEs in the whole Mediterranean basin refer to international volumes and publications, and references therein (e.g., [11,55,67,68,74–77]).

In order to define the contribution of the most important commercial deep-sea species as food resources from the depths of the Mediterranean Sea, landing data from official FAO statistics were explored (https://www.fao.org/fishery/statistics-query/en/gfcm\_capture/ gfcm\_capture\_quantity, accessed on 12 January 2022), focusing on the central part of the basin (Figure 1).

**Figure 1.** Average total landing (L) of deep-sea commercial species for each FAO Mediterranean subdivision, expressed in tonnes (t) and percentages (%), calculated for the period 1994–2019. FAO subdivisions are coded as Balearic (BAE, 1.1), Gulf of Lion (G. Lion, 1.2), Sardinia (SAR, 1.3), Adriatic (ADR, 2.1), Ionian (ION, 2.2), Aegean (AEG; 3.1), and Levant (LEV, 3.2).

The temporal trends over a period of 25 years (1994–2019) were analysed by means of Spearman's non-parametric correlation.

New observations from the central Mediterranean, the southwestern Adriatic, and the northwestern Ionian, as well as on muddy bottoms of the northwestern Ionian Sea, were derived from data collected as part of national and international study projects carried out in the last two decades by the ecology team from the Department of Biology at the University of Bari Aldo Moro. In particular, data from deep-sea sensitive habitats and VMEs were taken using different low-impact fishing techniques [12,71,78–85], while data from muddy bottoms were collected during the Mediterranean Trawl Surveys (MEDITS) programme, included in the EU Data Collection Framework to date [86]. The MEDITS surveys are carried out in the Mediterranean from late spring to summer every year, according to a standardised protocol that includes gear characteristics, haul duration, and sampling procedures, following a depth-stratified random design, from 10 to 800 m in depth [86–89].

Using MEDITS data, the abundances in weight (expressed as biomass index kg/km2) and numbers (expressed as density index N/km2) of the deep-sea species distributed on deep muddy bottoms (200–800 m) of the northwestern Ionian Sea (Figure 2) were evaluated for the period 1994–2020, and their changes over time were tested using Spearman's nonparametric correlation. Data on the sea-bottom temperature (SBT) were recorded using a probe at the start and the end of different MEDITS hauls carried out from 1998 to 2020, and an average value of SBT was computed per year. The fishing pressure of bottom trawling fleets on the resources of the northwestern Ionian Sea was analysed using fishing effort (FE) data, in terms of number of vessels and gross tonnage (GT). Data were obtained from the European Fishing Fleet Register (http://ec.europa.eu/fisheries/fleet/index.cfm, accessed on 12 January 2022) for the period 1994–2020. The relationship between abundance of the deep-sea species and SBT was evaluated using linear regression analysis. Spearman's non-parametric correlation was also applied to the abundance data in weight (kg/km2) of the deep-sea species that showed a significant trend over time versus the FE—expressed as the total annual number of vessels—throughout the study period.

**Figure 2.** Topographic features, highs, banks, canyons, sensitive habitats, and VME species and habitats along the southwestern Adriatic Sea and northwestern Ionian Sea (central Mediterranean). GS = Gondola Slide; BC FRA = Bari Canyon Fisheries Restricted Area; SML FRA = Santa Maria di Leuca Fisheries Restricted Area; TC = Tricase Canyon; GC = Gallipoli Canyon; TT = Taranto Trench; AS = Amendolara Shoal; CB = Crotone Bank; SGCS = Squillace Gulf Canyon System; PSB = Punta Stilo Bank; SCCS = South Calabria Canyon System; SMC = Strait of Messina Canyon; triangle = hard bottom corals; asterisk = hard- and soft-bottomed corals [58,81,90–97]; lined areas *= Isidella elongata* facies [98]; NA = sampling area near the SML FRA; FA = sampling area far from the SML FRA.

Furthermore, for the shrimps *A. foliacea* and *P. longirostris*, due to correlation between environmental covariates (*ρ* = −0.73, *p* < 0.001), and in order to avoid multicollinearity problems, linear regression models were estimated to investigate the dependence between log-transformed abundances and environmental drivers (i.e., SBT and FE). Transformed responses ensure, in these cases, that the model assumptions are met. For both species, *s* = {*A. foliacea*, *P. longirostris*}, and for each *yz* with *z* = {abundance in weight, abundance in number}, the linear model is specified as follows:

$$\log(y\_z^{(s)}) = \mathcal{B}\_0^{(s)} + \mathcal{B}\_1^{(s)} \mathbf{x}\_i^{(s)} + \mathbf{e}^{(s)} \tag{1}$$

where *xi* represents the independent covariate, with *i* = {FE, SBT}.

Using linear regression analysis, the relationship between length and depth was evaluated for *M. merluccius*, *P. bogaraveo*, *P. blennoides*, *H. dactylopterus*, and *Galeus melastomus*, collected both on muddy bottoms with the MEDITS trawl net and in VMEs with an experimental longline (e.g., [81]), and the boxplots of the length were represented for all of these species in both habitats.

In order to detect an effect of the presence of a VME on fishery resources, MEDITS abundance data on the weight and number of the species *A. foliacea*, *P. martia*, *M. merluccius*, *P. bogaraveo*, *P. blennoides*, and *H. dactylopterus*, for an area near the Santa Maria di Leuca (SML) cold-water coral (CWC) province (NA), were compared with those of other species far from this coral province (FA) (Figure 2). Data from 54 trawl hauls, carried out between 200 and 800 m, were used for each area. Relative boxplots of the abundances in weight and number were produced, and the differences in the abundances between the two areas were tested using the Kruskal–Wallis non-parametric test. The pressure of fishing activity in these two areas was assessed in order to exclude effects due to this activity on the results of the comparison between the two areas. Specifically, FE was calculated for NA and FA by aggregating the fleets operating close to the two areas. In particular, the fleets of Gallipoli, Leuca, and Otranto were considered for NA, while those of Corigliano Calabro and Cirò Marina for FA. The differences in the species abundances between the two areas were tested using the Kruskal–Wallis non-parametric test.

### **3. Review of the Mediterranean Studies on the Link between Deep-Sea VMEs and Fishery Resources**

In the Mediterranean Sea, the deep-water resources are mainly exploited by trawl fishing on the soft bottoms of the bathyal grounds. However, there are areas characterised by the occurrence of VME species on soft and hard bottoms, canyons, and seamounts, where the fishing is carried out using different types of gears.

### *3.1. Open Slope, Soft Bottoms*

Between the shelf break and descent to bottoms deeper than 1000 m, soft corals can be found that can form dense aggregations on soft bottoms—called sea pen fields, sea fan corals, and arborescent corals—which build up coral gardens or coral forests. Coral gardens can develop on soft or hard substrata, depending on the habitat-forming species. Both sea pen fields and coral gardens and/or coral forests contribute to making more heterogeneous and complex habitats, attracting mobile and swimming fauna [55].

The sea pen fields built up by the octocoral *Funiculina quadrangularis* are mostly distributed on the upper slope, generally at less than 400 m in depth, on soft muddy habitats characterised by noticeable bottom currents. These habitats are commonly inhabited by commercially valuable crustaceans, such as the deep-water rose shrimp (*P. longirostris*) and the Norway lobster (*N. norvegicus*). Soft-bottomed coral gardens, structured by the gorgonian *Isidella elongata* (bamboo coral), can be found from the shelf break down to 1600 m. The valuable deep-water red shrimps (*A. antennatus*, *A. foliacea*) and the golden shrimp (*P. martia*) are frequently associated with these coral gardens [11,54,66,99–101]. Bamboo coral seems to play a role in habitat formation, increasing the three-dimensional habitat complexity on flat bathyal bottoms with its candelabrum-like shape. As a passive feeder, its occurrence is often associated with plankton-rich currents which, in turn, favours a high density of prey, such as pandalid shrimps and other crustaceans [102–104]. These prey animals attract predators of different trophic levels, such as the abovementioned deep-water red shrimps, bony fishes (e.g., *M. merluccius*, *P. blennoides*, *H. dactylopterus, P. bogaraveo, L. boscii*), and sharks, such as the lesser spotted dogfish (*Scyliorhinus canicula*) and the blackmouth catshark (*G. melastomus*), along with cephalopods (e.g., *I. coindetii*, *T. sagittatus*, *T. eblanae*), all of commercial interest [70,98,105–107]. In addition to the important implications as a feeding area for bentho-pelagic species, the arborescent complexity of the colonies could further act as shelter and spawning/nursery sites for several species that can grow to greater sizes than in areas where bamboo coral does not occur [98,104,107,108]. The

commercial species associated with bamboo coral account for about 5% of all of the income of the professional fisheries in the Mediterranean [34], with increasing landings—especially in Italy and Spain—the main producers in Europe [55,109].

### *3.2. Open Slope, Hard Bottoms*

Coral gardens or coral forests between the shelf break and upper slope are mainly made up of antipatharians and alcyonaceans. Among the former, the most widespread species are *Antipathes dichotoma*, *Parantipathes larix*, *Leiopathes glaberrima,* and *Antipathella subpinnata*, which form monospecific or multispecific forests [54,55]. Several commercial fish species are often associated with these antipatharians (e.g., [52,108,110]). Alcyonaceans are present on Mediterranean Sea with hard bottoms with several species, covering a wide bathymetric range. The whip-like gorgonian *Viminella flagellum* and the fan-shaped gorgonian *Callogorgia verticillata* are present in the bathyal zone at depths from 100 to 500 m and from 150 to 1000 m in depth, respectively [54,55]. Off the southwestern coasts of Sardinia, several fish species—some of commercial interest—have been observed hiding among the colonies of *L. glaberrima*, while egg capsules of the shark *S. canicula* have been found on the branches of this antipatharian at depths between 186 and 210 m [52,111]. The presence of egg capsules of this shark on *L. glablerrima* colonies had previously been observed on El Idrissi Bank (Alboran Sea) at 647 m and 452 m [112]. Cau et al. [111] suggested that the coral forest from a representative for southwestern Sardinia represent nursery grounds for *S. canicula*.

In the eastern Ionian Sea, the shark *G. melastomus* and the teleost fish *H. dactylopterus* were the most common fish species caught in the area, characterised by the presence of black coral (*L. glaberrima*) and bamboo coral (*Isidella elongata*) [108]. The shark seems to use the its habitat as a feeding area, and the teleost as a refuge area [108]; *H. dactylopterus* was also found together with other commercial fish species, such as the silver scabbardfish (*Lepidopus caudatus*), and the wreckfish (*P. americanus*) in a coral forest dominated by *L. glaberrima* on the Malta Escarpment (310–315 m) [113].

The fishes that coral zooxanthellate reefs produce in tropical waters account for 17% of animal protein consumed [114]. On the open slope of the Mediterranean Sea, there are still hard bottoms characterised by cold-water coral (CWC) communities, including solitary and colonial zooxanthellae cnidarians [94]. Colonial species have a complex branching morphology, and are habitat formers. The main species, known as white corals, are the colonial species *Madrepora oculata* and *Lophelia pertusa* (recently renamed as *Desmophyllum pertusum*), as well as the solitary coral *Desmophyllum dianthus*. These species have a broad frame-building ability, being able to deposit calcium carbonate and build up durable biogenic substrata. CWCs, as passive suspension feeders, depend on the supply of current-transported particulate organic matter and zooplankton for their trophic requirements. They are preferentially distributed on topographic irregularities on the slope, in canyons and on seamounts, where there are strong currents and the sedimentation rate is low [53,91,115–117].

CWC habitats are impacted by fishing due to the occurrence of large sizes and high abundances of commercial species [9,10,13,16,18,58,70,118,119] and references therein]. The presence of corals is generally known to the local fishers, who experience gear damage and losses, although they often fish close to these areas with the aim of obtaining a greater catch and larger specimens of valuable commercial species, such as the deep-water red shrimps (*A. antennatus* and *A. foliacea*) and the European hake (*M. merluccius*). In fact, side-scan sonar and underwater video images show the characteristic seabed scars of otter trawls ploughing through the coral banks [12,82]. Longline is also used in these areas of complex bottom topography, and is not accessible to trawling, so as to catch wreckfish, greater forkbeard, blackbelly rosefish, blackspot seabream, and bluntnose sixgill shark [71,78,81].

CWC habitats provide a suitable ground for larval settlement and juvenile growth of benthic species. They are spawning and nursery areas for vagile and swimming

fauna, acting as an EFH for several commercial and non-commercial fish and invertebrate species [12,17,57,71,78–81,83,84,111].
