The North sector of the Strait of Sicily: a priority area for conservation in the Mediterranean Sea
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The largest semi-enclosed basin in the world, the Mediterranean Sea, is characterized by high biodiversity and heavy human pressure on the coastal system. The Strait of Sicily (SoS) represents the boundary between western and eastern Mediterranean sub-regions and is an important biodiversity hot spot. Given its ecotonal nature and it being a “crossroad” for the westward expansion of warm-temperate and tropical species from the Levantin basin, the SoS is likely to play a key role in future climate change related biodiversity changes within the Mediterranean. The complexity of the SoS ecosystem, characterized by wider shallow detritic and rocky banks on the continental shelf hosting large biodiverse communities, and peculiar circulation pattern, promotes species diversity and abundance. In addition, the deep-sea is characterized by the occurrence of extremely vulnerable habitats, such as deep-water communities of scleractinian corals, antipatharians, gorgonians, and red coral. We review the current knowledge on the main characteristics of the north sector of the SoS ecosystem. The SoS ecosystem is increasingly threatened by expanding anthropogenic pressures in the area and specific conservation measures should be implemented on a national and international level to protect the relevant and vulnerable habitats.
KeywordsMediterranean Sea Strait of Sicily Biodiversity Conservation Fishery
Prominent features in the SoS are: deep coral assemblages (Consoli et al., 2016), pockmark fields and fossil cold seep communities (Taviani et al., 2013), coralligenous habitats, rare or endemic species, high habitat heterogeneity, spawning and nursery grounds for demersal and large pelagic fish, persistent diversity hotspots of demersal species, and large fluxes of Atlantic and Indo-Pacific exotic species (García Lafuente et al., 2002; Garofalo et al., 2007; Fortibuoni et al., 2010; Colloca et al., 2015). From a biogeographic point of view, the SoS is considered the connection between the western and the eastern Mediterranean basins and is marked by the 15°C isotherm crossing the eastern area in February. This isotherm is recognized as a sort of “physiological” barrier to the westward expansion of warm-affinity species occurring in the Eastern Mediterranean basin (Bianchi, 2007; Garilli, 2011), the presence of which determines a clear change in species composition between the west and east sectors of the SoS (Bianchi, 2007).
The SoS is also identified as a Mediterranean biodiversity hot spot due to the occurrence of complex and diversified benthic biocoenoses (Garofalo et al., 2007; Consoli et al., 2016). Coll et al. (2010) found around Sicily the greatest richness of marine vertebrate (375 species per 0.1 × 0.1 degree cell) in the Mediterranean Sea. Other studies have shown a high diversity and biomass of demersal communities over the offshore detritic bottoms of the Adventure bank (Gristina et al., 2006; Garofalo et al., 2007). Such high diversity is also linked to the “crossroad” nature of the SoS for species of distinct tropical or subtropical origins (Atlantic and Indo-Pacific), expanding their range longitudinally into the Mediterranean (Azzurro, 2008; Lejeusne et al., 2010). The ecotonal nature of the area is well illustrated by the co-occurrence of two species of the genus Charonia, one of the largest Mediterranean gastropods, C. lampas lampas (L.) typical of the western basin and C. tritonis variegata (Lamarck) which is widespread in the eastern basin (Bianchi, 2007). The area has been identified as a priority for conservation by de Juan et al. (2012) and Oceana (2011) with several sites identified for future inclusion in a Mediterranean network of marine protected areas (MPAs), including: the Adventure Bank; Malta Bank; Urania Bank; Linosa Bank; and Southern Sicilian seamounts. In 2014 the SoS was identified as an Ecologically or Biologically Significant Area (EBSA) by the Contracting Parties of the Convention on Biological Diversity (Bax et al., 2016).
Crucially the Mediterranean is facing increasing stress due to the intense pressure from a variety of human activities. The SoS is the most important traffic lane for oil tankers crossing the Mediterranean East–West towards the Black Sea, Suez and Gibraltar (Patruno, 2008). Additionally, there is increasing demand for oil drilling and mining in the area. Traditional activities, such as fishing, are extremely important for local communities, yet most of the commercial stocks have been overexploited (FAO, 2016).
Given the pressing need to implement a comprehensive and effective conservation plan for the SoS, the aim of this work sets out to provide decision makers with an in-depth review of the existing knowledge and main characteristics of the north sector of the SoS ecosystem, giving particular attention to those habitats and species considered to be of greatest importance when designing and deciding upon the most appropriate conservation strategies.
The SoS is characterized by a narrow continental shelf in the central part with extensions off the eastern (Malta Bank) and western Sicilian coasts (Adventure Bank). The slope shape is extremely irregular, with many trenches steep declines, and seamounts that are cut off by sub-horizontal and more accessible trawlable areas (Consoli et al., 2016). The sea bottom has emerged several times during its geological history (Civile et al., 2015). The last emergence was during the Early Holocene and caused the formation of small islands that punctuated the Adventure bank, forming a broad archipelago, now located between 10 and 40 m. They are composed either of sedimentary rocks (Talbot, Ante-Talbot, Nereo, and Pantelleria Vecchia banks), or represent submarine Pleistocene volcanic edifices (Galatea, Anfitrite and Tetide banks; Civile et al., 2015; Fig. 1).
The shelf is characterized by the inflow of terrigenous material from the Atlantic Ionian Stream (AIS) which forms a wedge of well-stratified sands and silty shale with thickness varying from 56 m near the coasts to almost zero at the edge of the shelf (Colantoni et al., 1985). An exception is the Adventure Bank, which is characterized by a virtually flat surface with a mean depth of about 80–90 m. The Adventure Bank is not affected by the inflow of terrigenous material because of a strong current regime. As a consequence, the sediment deposition in the Adventure Bank is biogenic: (1) carbonate sands consisting mainly of the remains of organisms (bryozoans, red algae, serpulidae, foraminiferidae, gastropods and corals) living in the extensive seagrass and seaweed meadows; and (2) fragments of biogenic concretions (coralligenous) (Colantoni et al., 1985).
Past volcanic activity in the SoS produced several seamounts (Tetide, Anfitrite, Galatea, Cimotoe, Graham, Bannock and Nameless Bank), creating the conditions that support a diversity of important habitat types. Two of which emerged to form the Pantelleria and Linosa Islands (Calanchi et al., 1989). Neogene rifting caused the development of three major depressions, the Pantelleria (1,317 m depth), Linosa (1,529 m depth), and Malta (1,731 m depth) depressions, located in the central part of the SoS (Civile et al., 2008). The Graham Seamount is an active volcano characterized by lava flows and fumaroles along the north eastern flank at depths ranging from 160 to 50 m (Civile et al., 2008). Shallow-sea mud volcanoes were recently reported along the continental shelf of the Malta plateau offshore Sicily (Holland et al., 2003; Savini et al., 2009).
Oceanography water circulation: eddies, vortices, fronts, and environmental features
Broad scale climate and oceanographic features and drivers
Key biological aspects
Primary production and zooplankton
Chlorophyll measures in the SoS ranged between 14 and 60 mg m−2 in the 0–100 m depth stratum (Nardello et al., 2004). Primary productivity, expressed as mg m−2 of carbon is higher in the western sector of the area (Adventure bank) with values up to 524.61 mg m−2 day, between 0 and 20 m depth and the minimum value (218 mg m−2 day) in the south-eastern sector. Primary productivity showed a maximum value (524.61 mg m−2 day) between 0 and 20 m depth and the minimum value (110.94 mg m−2 day) at about 60 m depth (Nardello et al., 2004). Brunet et al. (2007) in a study carried out on vertical variability and diel dynamics of pico-phytoplankton in the SoS showed a deep fluorescence maximum (DFM) between 70 and 100 m. In the deep chlorophyll maximum (DCM), a significant diel periodicity was observed for the orange fluorescence (from phycoerythrin) and for the red fluorescence (from chlorophyll). The high pigment diversity of pico-phytoplankton in the DCM and its elevated contribution to total chlorophyll a indicated an elevated degree of adaptation to the quantity and quality of light available (Brunet et al., 2007). The phytoplankton community of the SoS has been scarcely investigated up to now. A past review highlighted that the contribution of pico-phytoplankton to primary production in the Mediterranean Sea varies from 31% in Straits of Messina to 92% in Ionian Sea; low values, instead, were found in the SoS (Magazzu & Decembrini, 1995).
Data from oceanographic surveys in the Eastern Mediterranean carried out at the beginning of the 90’s showed an increased abundance of meso-zooplankton in the SoS (Mazzocchi et al., 1997). The mean value recorded in the SoS was almost one order of magnitude greater than in the other areas (200 ± 47 ind. m−3). The zooplankton assemblage was dominated by copepods (81.83%), followed by ostracods (5.43%). In spring (reference period June 1999), zooplanktonic biomass values show a clear spatial pattern with high density values in the western sector of the area corresponding to upwelling areas and frontal systems. Three peaks, respectively off Sciacca (10.16 mg m−3), in front of Licata (6.38 mg m−3) and off Cape Passero (10.14 mg m−3), were evident (Cuttitta et al., 2003). The zooplanktonic biomass has shown higher values (expressed in Dry Weight; DW, mg m−3) in neritic stations than in pelagic and coastal waters (neritic areas: 6.08 ± 5.92 mg m−3; pelagic 4.35 ± 3.40 mg m−3; coastal 3.30 ± 1.75 mg m−3). The zooplanktonic community was dominated by copepods with 86 species (74.8% of total zooplanktonic organisms in 1999, 388.4 ± 233.5 ind.m−3; and 77.4%, 572.6; ± 362.9 in 2000) (Cuttitta et al., 2003).
In a recent study, a close biogeographic affinity of the benthos of the SoS with the benthos of the Tyrrhenian Sea was demonstrated (Massi et al., 2013). Yet, studies on the benthic communities in the SoS are few and scattered across different areas and periods, in particular the knowledge on the main benthic communities on the offshore banks are particularly scarce. Laminaria rodriguezii beds are frequent on the detritic and rocky bottoms of offshore banks under bottom currents, which also serve as nursery grounds for the catsharks Scyliorhinus canicula and S. stellaris (Suriano et al., 1992).
The “epibathyal” layer extends between 200 and 400–450 m, over generally muddy bottoms, with a consistent fraction of fine sand; biocoenoses are poorer and less varied than those of the circalittoral layer. The most typical species is the sea pen Funiculina quadrangularis, although in trawlable areas it is getting increasingly rare (Maynou & Cartes, 2012). The complex topography of SoS hosts various types of deep-sea carbonate sediments and rocks (Zibrowius & Taviani, 2005). The geo-biological exploration of deep-sea rocky bottoms located between 350 and ca. 800 m depth identified several sites with diverse deep-water scleratinian corals community, as well as large colonies of antipatharians and gorgonians (Zibrowius & Taviani, 2005).
Coralligenous communities, made up by complex assemblages of algal and animal constructors, characterize the circalittoral habitats along the Sicilian coast, the Pelagie Islands, and Maltese archipelago (Martin et al., 2014). These organisms are habitat formers and contribute to the structure of the SoS deep circa littoral and bathyal rocky bottoms, enhancing biodiversity and providing important ecosystem services including ecological niches, nursery areas, food and substrate for a variety of organisms (Rosso et al., 2010; Sanfilippo et al., 2013). In the SoS, deep rocky bottoms are characterized by several huge “buildings” produced by madrepores generally forming scattered clumps, which give origin to the “white coral assemblages” biocoenosis between 300 m and 450 m (Zibrowius & Taviani, 2005). White coral communities consisting of scleractinian corals were discovered during inspections of narrow shelves, canyon walls, escarpments, and seamounts below 200 m depth by remotely operated vehicles (Schembri et al., 2007; Freiwald et al., 2009; Taviani et al., 2011).
Numerous deep coral species are present in these areas such as Corallium rubrum (Linnaeus, 1758), Dendrophyllia cornigera (Lamarck, 1816), Desmophyllum cristagalli (Milne Edwards & Haime, 1848), the white corals Lophelia pertusa (Linnaeus, 1758), and Madrepora oculata (Linnaeus, 1758) as well as the black coral Leiopathes glaberrima (Esper, 1788) (Schembri et al., 2007; Freiwald et al., 2009; Taviani et al., 2009, 2011; Costantini et al., 2010; Deidun et al., 2010), at depths ranging between 90 and 800 m. The biodiversity associated with these habitats has been described in several studies (e.g., Zibrowius & Taviani, 2005; Schembri et al., 2007; Freiwald et al., 2009; Calcinai et al., 2013).
Fish and shellfish communities
Bluefin tuna, swordfish, and sharks
According to the results of larval campaigns, bluefin tuna (BFT) spawning occurs in several Mediterranean regions (Piccinetti et al., 1997), with remarkable concentrations of eggs and larvae occurring off the eastern coast of Sicily. Oray et al. (2005) showed the results of a 2003 and 2004 fish egg and larval survey over the BFT spawning grounds off the southern Sicilian coasts (SoS). Traditional fishing activities (“tonnare”) have been replaced in recent years by purse seine and longlines; regulated under a quota system that varies annually.
Swordfish (Xiphias gladius) is the second most important of the large pelagic species in the Mediterranean Sea. The International Commission for the Conservation of Atlantic Tunas (ICCAT) considers the existence of a single Mediterranean stock for this species, with the SoS shown to be the most important spawning grounds for the species (Wurtz, 2010; Di Natale, 2006).
The SoS area also represents a biodiversity hot spot for a great number of shark species, some of which have become rare or are no longer present in other sectors of the Mediterranean (Bradai, 2012). The Mediterranean hosts a resident and genetically distinct population of white shark (Carcharodon carcharias) and the SoS is one of the most important spawning areas of the species in the region (Saïdi et al., 2005; De Maddalena & Heim, 2012). The sandbar shark (Carcharhinus plumbeus) concentrates seasonally around the Pelagie Islands; a major attraction for divers in this region.
Anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) are the two most important small pelagic species supporting local fisheries. Their biomass and distribution is estimated annually through acoustic pelagic surveys (MEDIAS programme). In the north sector of SoS, both sardine and anchovy undergo large inter-annual fluctuations with biomass estimates ranging from 6,000 to over 36,000 tons and 7,000–23,000 tons, respectively (Patti et al., 2004; Fiorentino et al., 2013). The spatial distribution of anchovy spawning areas in the north sector of the SoS is determined by several factors including water temperature, water column stability, and fluorescence (Basilone et al., 2013). Shallow waters with upwelling (low temperature, high fluorescence) and moderate current speeds provide preferred areas for spawning (Basilone et al., 2006).
The SoS is one of the areas with the greatest demersal species richness in the Mediterranean basin (Gaertner et al., 2007; Coll et al., 2010). The composition of demersal species assemblages is reported by Gristina et al. (2006) who also evaluated the impact of fishing on the community in terms of species composition and biomass. Similar studies were carried out in Maltese waters, where significant differences in terms of species diversity and abundance were detected between protected and unprotected areas, the former hosting twice as much biomass as well as larger individuals of some species than the latter (e.g., elasmobranchs; Dimech et al., 2008). The area is characterized by a rich community of elasmobranchs and hosts the largest number of species in the north Mediterranean Sea (37 species recorded by Relini et al., 2000; Bertrand et al., 2000) some of which (e.g., Mustelus mustelus, Raja clavata) are also important for demersal fisheries (Garofalo et al., 2003; Ragonese et al., 2013). The greatest fish diversity was found on the offshore bank on the western part of the south Sicilian shelf (Adventure Bank, Garofalo et al., 2007). In this area, fish diversity increases consistently with habitat complexity and it is characterized by the occurrence of uncommon and poorly known species as well as the aggregation of vulnerable elasmobranchs, such as Myliobatis aquila (Consoli et al., 2016). Habitat heterogeneity appears to be a key factor controlling the abundance and diversity of demersal elasmobranchs in the area (Lauria et al., 2015).
The continental slope, at deeper than 200 m in the Adventure Bank, is dominated by soft-bottom communities characterized by decapod assemblages (Ragonese et al., 2009), including species of tropical or subtropical origin (e.g., giant red shrimp: Aristaeomorpha foliacea, deep-water rose shrimp: Parapenaeus longirostris). The analysis of the temporal trend in biomass and density of bathyal species recorded during trawl surveys carried out since 1994 show an increasing number of cephalopods and elasmobranchs and a stable pattern for crustaceans and bony fish (Gancitano et al., 2016). Several studies have addressed juvenile commercial fish and shellfish spatio-temporal distribution in the SoS area with the main aim to identify nursery areas (e.g., Fiorentino et al., 2003; Fortibuoni et al., 2010; Garofalo et al., 2010, 2011; Colloca et al., 2015). The studies found the outer edges of the Adventure and Malta banks to play a key recruitment role of important commercial species such as hake (Merluccius merluccius) and deep-water rose shrimp in relation to the pattern of larval transport and retention (Garofalo et al., 2011).
Birds, mammals, sea turtles
The SoS area represents an important area of migration passage for large cetaceans. The cetacean fauna of the area is rich. Fin whales (Balaenoptera physalus) are known to congregate in the coastal waters of Lampedusa Island to feed on the euphausiid Nyctiphanes couchii in late winter—early spring (late February–early March) (Canese et al., 2006; Aissi et al., 2008). Sperm whale (Physeter macrocephalus) occurs round the year. Several studies document the distribution and abundance of different cetaceans, such as the bottlenose dolphin (Tursiops truncatus), common dolphin (Delphinus delphis), and striped dolphin (Stenella coeruleoalba) in the area (see UNEP-MAP-RAC/SPA, 2014; Vella & Vella, 2012). Resident populations of the bottlenose dolphin are present around Lampedusa (Pulcini et al., 2013) and along the western coasts of Sicily where a population of 103 individuals was monitored (Papale et al., 2017). The SoS is one of the most important areas for the loggerhead turtle (Caretta caretta) with important nesting sites in Lampedusa and Linosa (two Natura 2,000 sites) and along the Sicilian coast (Mingozzi et al., 2007; Casale et al., 2014). Since 1995, more than 600 sea turtles have been marked and released by the sea turtle rescue center in Lampedusa. A study carried out in the period 2000–2008 showed fishing is the main source of mortality for loggerhead turtles in the area especially from longlines (Casale et al., 2007; Casale et al., 2010). The island of Linosa hosts one of the largest colonies of the Cory’s Shearwater (Calonectris diomedea) the Mediterranean (Brichetti and Fracasso, 2003).
Threats to SoS biodiversity
Fisheries in the North sector of the SoS (Italy and Malta), as in other Mediterranean sectors, are mixed, with a high number of stocks exploited and several different fishing gear used. The Italian fleet in the South of Sicily consists of about 390 trawlers exploiting different fishing grounds from the outer shelf, where mixed assemblages of fish and cephalopods are targeted, to the bathyal bottoms on the middle slope (400–600 m) to target giant red shrimp (Aristaeomorpha foliacea). On the upper slope (200–400 m), trawlers target deep-sea rose shrimp (Parapenaeus longirostris) with hake (Merluccius merluccius) being the main commercial by-catch species. A description of the spatial distribution of the fishing effort exerted by trawlers in the SoS can be found in Russo et al. (2014). Between 2004 and 2015, the effort exerted for bottom trawl fishing by Italian trawlers decreased by 41% with a 38% reduction in annual landings. In 2011, the Maltese fleet consisted of 12 trawlers (4 of 12–24 m and 8 over 24 m), 11 of which were licensed to operate within the 25 nautical miles Maltese Fisheries Management Zone (Fisheries Management Plan). The artisanal fleet is also important locally exploiting a wide range of species using different fixed gears (e.g., longlines, trammel nets, gillnets).
The other important fishery in the area is the pelagic fisheries; targeting small pelagic fish (anchovy and sardine) with about 20 active purse seine vessels in spring–summer, and 15 mid water pair trawlers. A seasonal fishery, specifically targeting dolphinfish (Coryphaena hyppurs), using Fish Aggregating Device, (“FADS”) operates in September–October.
The most important commercial species in the area is the deep-sea rose shrimp (Parapenaeus longirostris) with landings between 5,000 and 10,000 tons/year. Followed by the giant red shrimp, sardine, European hake, anchovy, and swordfish. The assessment of the status of the stocks in the region is carried out both by the working groups of the Food and Agriculture Organization of the United Nations (FAO) and the General Fisheries Commission for the Mediterranean (GFCM), which plays a key role in fostering the development of assessment on shared stocks between EU and non-EU countries also in cooperation with the FAO regional project MedSudMed. The results of the assessments carried out in the last years pointed out a general condition of overfishing of the main commercial stocks (Colloca et al., 2013; FAO, 2016). The only stock that resulted as sustainably exploited was the Norway lobster (Nephrops norvegicus).
Maritime traffic and tourism
The SoS is the most important traffic lane for crude oil crossing the Mediterranean. Traffic is intense as it connects the east and west basins and the Black Sea, Suez and Gibraltar. The concentration of oil tanker traffic is close to 80% of the total in the whole region (Patruno, 2008). For this reason, SoS is considered to be at very high risk of pollution from ships, in a region where, between 1978 and 2003, 470 accidents were recorded with 305,000 tons of oil and 136,000 tons of various chemical products discharged at sea. Furthermore, although the Mediterranean is recognized to be a special area by the MARPOL Convention (Peet, 1992), where any discharge of oil or oily residues and mixtures from ships is prohibited, the so-called operational pollution, which is the marine pollution arising from routine shipping activities and voluntary discharges, have recently become much more significant (Patruno, 2008).
Tourism is one of the most important economic activities in Sicily and Malta. Coastal areas are under extremely high touristic pressure, especially during the summer months. Urbanization of the coast for the creation of touristic infrastructures (e.g., resorts, marina, etc.) is having increasing impacts on fragile coastal habitats such as P. oceanica meadows. Large touristic presence often overlaps with the breeding areas of endangered or fragile species; having led to the near extinction of the monk seal Monachus monachus and pose a real threat to endangered species such as the sea turtle Caretta caretta (Giacoma & Solinas, 2001).
The SoS is recognized as one of the main hotspots for recording alien species in the Mediterranean and small islands, such as Linosa, may act as stepping stones for the secondary dispersal of non-native species from west to east Mediterranean basin or vice versa (Occhipinti-Ambrogi et al., 2010). The area is considered as a strategic observation outpost for the monitoring of marine non-indigenous fish species (Azzurro et al., 2014). These include species known from the Eastern Atlantic coasts might have extended their range through Gibraltar as well as entering the Mediterranean through the Suez Canal and/or may have been introduced by human activities (Azzurro et al., 2014). The ongoing warming trend has substantially accelerated the arrival and acclimatization of non-indigenous (NIS) thermophilic species, including macroalgae (e.g., Caulerpa racemosa, Asparagopsis taxiformis; Occhipinti Ambrogi et al., 2011) but also invertebrates and fishes. The increase in water temperature is causing a shift in the thermal habitat suitability, favoring warm-affinity invasive species competing with indigenous ones (Marras et al., 2015).
A recent study in Maltese waters identified 66 NIS with a dominance of molluscs (21 species), fish (15 species), crustaceans (8 species), and algae (7 species) (Evans et al., 2015). Seven of these species (Caulerpa cylindracea, Lophocladia lallemandii, Womersleyella setacea, Brachidontes pharaonis, Percnon gibbesi, Fistularia commersonii, Siganus luridus) are considered to be invasive (Evans et al., 2015). Whereas the number of NIS found in the SoS area is increasing exponentially, the direct and indirect impacts on the ecosystem and economic coastal activities are still unclear. Although some advantages for local fisheries might derive from the increase of new commercial species (i.e., Scannella et al., 2017) many species can produce negative impact through ecological processes such as competition, predation, and trophic cascade (Bax et al., 2003; Galil, 2007). Evidence of climate change effects on benthic communities have been illustrated by temporal change in benthic algae composition, with an increased importance of thermophilic species and a decrease in the species with cold water affinity (Alongi et al., 2004).
Gas pipelines, oil drilling, and renewable energy
Deployment of pipes and cables for gas, water transport, communication, and renewable energy (e.g., wind turbines) represent another major anthropogenic pressure of increasing concern. To our knowledge, only a few peer-reviewed studies considered these kinds of human impacts within SoS. Particularly, a recent study (Badalamenti et al., 2011) highlighted the impact of gas pipelines on P. oceanica on the western side of the SoS. This area is characterized by some of the largest P. oceanica meadows in the Mediterranean Sea. One of these meadows was recently strongly impacted by the deployment of a gas pipeline between Cape Bon (north east Tunisia) and Cape Feto (south west Sicily, Italy), which led to a removal by dredging of a large portion of P. oceanica altering the original substrate, with consequences along the entire ecosystem, and increasing the recovery time of the meadow (Badalamenti et al., 2011).
Oil drilling is another important activity in the offshore area of the south coast of Sicily carried out by six oil platforms extracting annually about 280.000 tons of oil from 36 wells. It is an expanding activity, which has recently led activists and politicians to protest against future plans by international companies to further prospect for oil (https://www.ft.com/content/77ab5168-a3ee-11df-9e3a-00144feabdc0). Most of the permission requests for new drilling activity are in areas within or close to protected areas or priority areas for conservation, thus increasing the risks for being able to best safeguard the coastal marine environment.
Renewable energy in the oceans is becoming crucial in the EU energy policy (Magagna & Uihlein, 2015) and the Horizons 2020 EU Renewables Directive (2009/28/EC) calls member states to obtain 20% of their energy consumption from renewable energy sources by 2020. As a side effect, there is an increasing demand for the deployment of offshore wind power in EU waters to help reduce carbon emissions. However, several studies documented major environmental concerns related to offshore wind developments such as, physical destruction of seabed habitats, increased noise levels, changes to benthic and pelagic habitats, alterations to food webs, and pollution from increased vessel traffic or release of contaminants from seabed sediments (Bailey e al., 2014). Although the Mediterranean Sea has no operational offshore wind farms yet, their expansion in the next years is probable (Bray et al., 2016). The SoS and in particular the Adventure Bank is considered a candidate site for wind power deployment due to wind resource availability and low depths (Bray et al., 2016). Until now, official requests for the deployment of offshore wind farms in Italian national waters (Adventure Bank and Pantelleria Bank) have been rejected by both the Italian Ministry of Environment and the Sicilian Region Administration due to the occurrence of protected habitats (e.g., P. oceanica meadows). It is, however, likely that an increased demand for wind farms and concessions will produce new sources of conflicts amongst coastal resource users.
This review highlights that the SoS is a biologically important area in the Mediterranean Sea. High diversity could be linked firstly to, high habitat complexity structured by several offshore banks which support a high species diversity (Consoli et al., 2016), and secondly, the ecotonal nature of the SoS with the overlapping distribution of species typical of the western and eastern Mediterranean basin (Bianchi, 2007). Global warming has also enhanced the role of this area as a “crossroad” for species of distinct tropical origins (Atlantic and Indo-Pacific), expanding their range longitudinally within the Mediterranean (Azzurro, 2008; Lejeusne et al., 2010) and potentially providing a more suitable thermal habitat to invasive species (Marras et al., 2015).
The increased productivity of the SoS area, particularly around the shelf break of the two main banks, the Adventure and Malta banks, produces density hotspots of juveniles of several important commercial species, such as European hake, deep-sea rose shrimp, and broadtail shortfin squid (Fiorentino et al., 2003; Garofalo et al., 2011; Colloca et al., 2015). In this respect, the Atlantic Ionian Stream has a crucial role in the generation of a number of semi-permanent upwellings, eddies, and fronts which enhance and concentrate marine productivity (Agostini & Bakun, 2002). The observed stable highly productive patches of juveniles of different species are linked to the occurrence of three major classes of physical processes combining to yield favorable reproductive/recruitment habitats for fish following the “fundamental triad” of Bakun (1996), namely: (i) enrichment processes (i.e., permanent upwelling to the left of the Atlantic Ionian Stream: AIS); (ii) concentration processes (convergence, frontal formation, water column, stability); and (iii) processes favoring retention within or drift toward appropriate habitats (AIS meanders and gyres around the banks). Additionally, the offshore banks are some of the few areas in the Mediterranean still hosting high biodiversity of elasmobranchs with the occurrence of spawning/mating and nursery areas for threatened species (Ragonese et al., 2013; Lauria et al., 2016; Colloca et al., 2017). The conservation of these residual elasmobranch populations is essential in a region such as the Mediterranean; an area characterized by the highest proportion of threatened species (Dulvy et al., 2014).
Coralligenous communities, made up by complex assemblages of habitat constructing flora and fauna, are characteristic of the circalittoral habitats along the Sicilian coast, the Pelagie Islands and Maltese archipelago (Martin et al., 2014). The Barcelona Convention’s ‘Action plan adopted in 2008 for the conservation of coralligenous outcrops and other calcareous bio-concretions in the Mediterranean Sea’ assert that “coralligenous/maërl assemblages should be granted legal protection (UNEP-MAP-RAC/SPA, 2008). Maërl communities, also occurring in some areas near Malta and on offshore banks, are protected by the EU Mediterranean regulation 1967/2006 banning the use of towed gear on these habitats. Because of their extent, biodiversity and production, macroalgae characterize the detritic and rocky bottoms of the offshore banks under specific bottom currents. The occurrence of Laminaria rodriguezii beds is frequent, and they can serve also as nursery grounds for the catsharks Scyliorhinus canicula and S. stellaris (Suriano et al., 1992). L. rodriguezii, a paleoendemic species included in the annex I of Bern Convention and annex II of the SPA/BIO Protocol of the Barcelona Convention, is extremely sensitive to fishing activities and changes in ecological conditions (Relini & Tunesi, 2009).
The SoS provides important nesting sites for loggerhead turtles (Caretta caretta) in the central Mediterranean, whilst also providing an important dispersion/migration route for the species (Bentivegna et al., 2007). The cetacean fauna is rich and diversified with important resident populations of bottlenose dolphins Tursiops truncatus (UNEP-MAP-RAC/SPA, 2014) and a seasonal feeding area for finwhale Balaenoptera physalis around Lampedusa island(UNEP-MAP-RAC/SPA, 2014). The finwhale is classified as “endangered” by the IUCN and it is protected under the Endangered Species Act (ESA) and the Marine Mammal Protection Act (MMPA). Finally, the SoS is a well-known area of occurrence of large pelagic predators: such as sharks, including the, white shark, bluefin tuna; and swordfish.
Conservation priorities and measures enforced
For all the above mentioned reasons, the SoS region has been prioritized for conservation by de Juan et al. (2012) and Oceana (2011) with several sites identified for future inclusion in a Mediterranean network of MPAs, including: the Adventure Bank, Malta Bank, Urania Bank, Linosa Bank, and Southern Sicilian seamounts. In actuality, the Contracting Parties of the Convention on Biological Diversity (CBD) recognized the whole SoS as an Ecologically or Biologically Significant Area (EBSA) at international level in 2014. In addition, the RAC/SPA (Regional Activity Centre for Specially Protected Areas) is considering the possibility to implement one or more Specifically Protected Areas of Mediterranean Importance (SPAMIs) to protect some of the offshore banks.
The main treaties for the protection of the marine environment in the Mediterranean are the: Convention for the Protection of the Marine Environment; the Coastal Region of the Mediterranean (Barcelona, 1976; amended in 1995), with its seven protocols; and the Agreement on the Conservation of Cetaceans of the Black Sea, Mediterranean Sea, and Contiguous Atlantic Area (Monaco, 1996; ACCOBAMS). Other measures with a direct effect on the conservation of Mediterranean habitats are included in EU regulations, for example, reg. 1967/2006 concerning the management of Mediterranean fisheries, which establishes the protection from certain types of fishing on seagrass beds, in particular, P. oceanica or other marine phanerogams, coralligenous habitats, and mäerl beds. In addition, the GFCM applies recommendations to reduce the impact of fishing on the ecosystem and species requiring special protection. One of the most important is the prohibition of fishing with towed dredges and trawl nets at depths beyond 1,000 m (Recommendation GFCM/2005/1). Other conservation measures applied in the area are related to the protection from trawling of the coastal shelf below 50 m depth or within the 3 nautical miles from the shore (Reg. EU 1967/2006). In 1971, Malta declared an Exclusive Fishing Zone (EFZ) that extended to 25 nautical miles from the baselines of the Maltese Islands (Act XXXII of 1971), in accordance with the United Nations Convention of the Law of the Sea. Within this area, now designed as a Fishing Management Zone (FMZ), trawling is permitted in designated areas, although the total trawling capacity within the 25 nautical mile zone will not be allowed to increase from its present level. Two MPAs have been designated, respectively, in the Pelagie Islands and Egadi Islands. Recently, the GFCM Commission has established a multiannual management plan for the fisheries exploiting European hake and deep-water rose shrimp in the SoS (REC.CM-GFCM/40/2016/4), which include the enforcement of three fisheries restricted areas where trawling will be prohibited (see Map in Fig. 5).
A more complex conservation strategy is also required to follow the three pillars of Blue Growth and for the achievement of the Development Millennium Goals, namely achieving ecological, economic, and social sustainability objectives for human activities in the area. The SoS is, in fact, highly exposed to the impact of different activities carried out along the shore (i.e., tourism, fishing) but also in offshore areas. Fishing is one of the traditional activities carried out by a main fleet of Italian trawlers, which operate alongside the other fleets (Tunisian, Maltese, and Egyptian trawlers) in offshore areas, including shallow shelf banks. Most of the main targeted stocks are in a state of overexploitation although some signs of recovery have been observed in the last years (Colloca et al., 2013; GFCM, 2015). For its role as a major Mediterranean traffic lane for crude oil, the SoS is considered as an area under very high risk of pollution from ships, with a high number of accidents recorded in the last years and tons of oil and various chemical products continually discharged at sea (Patruno, 2008). In addition, ballast water discharged from ships is one of the main vectors for the entrance of alien organisms (Hulme, 2007), as more and more frequently observed in Malta (Sciberras & Schembri, 2007), although the “International Convention for the Control and Management of Ships’ Ballast Water and Sediments” in 2004, aims at minimizing these type of impacts.
Mining and oil drilling are expanding activities that are in conflict with fisheries and due to the associated environmental risks are raising concern among conservationists (Consoli et al., 2013). Another threat on the SoS ecosystem is related to the increasing interest for the installation of wind farms on shallow offshore banks, often in areas where protected habitats occur (i.e., Posidonia oceanica).
Implications for conservation
An important case has been made for a further spatial conservation effort in the area where the need of minimizing the negative impact of human activities on the ecosystem should focus on the most important areas for conservation (e.g., areas in Fig. 5). By providing a summary of the existing knowledge, highlighting at risk areas, this review of the north sector of the SoS has the potential to contribute to the commitment to the Convention of Biological Diversity (CBD) to achieve a significant reduction in the current rate of biodiversity loss, protecting 10–30% of marine habitats by 2020. The EU Directive establishing a framework for maritime spatial planning (2014/89/EU) also provides an important tool for EU member states to plan their activities in national waters and to ensure their environmental sustainability. Different types of spatial conservation strategies can be designed to achieve this target. For example, the reduction of adverse impacts, primarily fishing, on nurseries and other essential fish habitats which are essential to allow the completion of a full life-cycle of a species (breeding, spawning, settlement, feeding, and growth to maturity) can also lead to economic benefits for local fisheries (Russo et al., 2014; Colloca et al., 2015; Di Lorenzo et al., 2016). The steps and processes required to move regional conservation plans towards implementation were discussed by Micheli et al. (2013) in particular in relation to political complexities, and specifically the feasibility of establishing collaborations among stakeholders in a complex region like the Mediterranean. This particularly applies to the SoS where most of the relevant habitats are in international waters making the adoption of agreed conservation planning extremely challenging due to differences in national legislations, policy priorities, stakeholders commitments and so on.
In this perspective, this review aimed to provide a baseline knowledge that can be useful for future development of a conservation effort, where one of the key elements should be the development of a network of MPAs (Roberts et al., 2003). However, in spite of the studies carried out on the SoS, the current knowledge on the spatial distribution of key habitats and threatened species is still poor. In this regard, there is a pressing necessity for more research to be conducted, as it is crucial to understand species life-history strategies such as movement and connectivity in order to identify critical habitats (i.e., nursery and spawning areas). Moreover, research efforts should go in the direction of promoting field studies that make use of non-destructive tools, such as Remote Operating Vehicles (Tessier et al., 2005; Porteiro et al., 2013) in particular for the exploration of the offshore banks and the identification of vulnerable habitats occurring in the region, helping avoid further unnecessary impacts on this unique and ecologically important area.
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