Mediterranean banks in EBSA area: Hotspots of biodiversity under threat

Mediterranean banks in EBSA area: Hotspots of biodiversity under threat

Marine Environmental Research xxx (2017) 1e12 Contents lists available at ScienceDirect Marine Environmental Research journal homepage: www.elsevier...

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Marine Environmental Research xxx (2017) 1e12

Contents lists available at ScienceDirect

Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev

Mediterranean banks in EBSA area: Hotspots of biodiversity under threat Chiara Altobelli a, Patrizia Perzia b, *, Manuela Falautano b, Pierpaolo Consoli c, Simonepietro Canese d, Teresa Romeo c, Franco Andaloro b a

Ministero dell’Ambiente e della Tutela del Territorio e del Mare (MATTM), Via Cristoforo Colombo 44, 00147, Roma, Italy  ISPRA, Institute for Environmental Protection and Research, S.T.S. Palermo, Lungomare Cristoforo Colombo, 4521 (Ex Complesso Roosevelt) Localita Addaura, 90149, Palermo, Italy c ISPRA, Institute for Environmental Protection and Research, Laboratorio di ittiologia ed ecologia marina, Via dei Mille 44, 98057, Milazzo, ME, Italy d  Marina, Via Vitaliano Brancati 60, ISPRA, Institute for Environmental Protection and Research, III Dipartimento Tutela degli Habitat e della Biodiversita 00144, Roma, Italy b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 February 2017 Received in revised form 7 September 2017 Accepted 9 September 2017 Available online xxx

This study demonstrates that, in the Central Mediterranean Sea, the Graham, Nereo and Pantelleria Vecchia Banks of the Strait of Sicily represent, in the wide and diversified ‘Sicily Channel’ Ecological or Biological Significant Area, unknown hot spots of biodiversity threatened by human activities. The investigated banks show an high ecological and biological value (EBV), assessed through presence/ absence of specific indicators. The ecological groups of Graham Bank show the maximum EBV; the same as Nereo and Pantelleria Vecchia, except for the benthic component. All three banks are highly threatened, mainly the benthic and benthopelagic ecological groups. However, these Banks still have wide pristine areas to protect and can be considered eligible sites for the imposition of area-based management measures of conservation. This study represent also a support for decision makers involved in protection of the Mediterranean open sea areas, to pinpoint other priority conservation banks. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Benthic ecology Biodiversity Conservation Convention on biological diversity Ecosystem evaluation Ecosystem-based management Mediterranean sea banks

1. Introduction Despite its high biodiversity value and the presence of areas of relatively high productivity, the open sea continues to be one of the least protected regions, also in the Mediterranean, where areas beyond national jurisdiction make up the largest part. The development of a network of Marine Protected Areas (MPAs) in the open seas is a challenging task, mandated by several international decisions, including the World Summit on Sustainable Development (Summit, 2002) and the Aichi Targets (COP 10 Decision X/2, 2010). Since 2008, the Regional Activity Center for Specially Protected Areas (RAC/SPA) has been contributing to promote this objective by

* Corresponding author. E-mail addresses: [email protected] (C. Altobelli), [email protected] isprambiente.it (P. Perzia), [email protected] (M. Falautano), [email protected] (P. Consoli), [email protected] it (S. Canese), [email protected] (T. Romeo), [email protected] isprambiente.it (F. Andaloro).

the MedOpenSeas project (MOS). The MOS is aimed at facilitating the establishment of Specially Protected Areas of Mediterranean Importance (SPAMIs), as defined in the SPA/BD protocol of the Barcelona Convention (United Nation Environment Programme and Mediterranean Action Plan, 1995), embracing open seas. In 2010, the first phase of the project led to the identification of twelve Priority Conservation Areas (PCAs) in the open seas, likely to contain sites, that could be candidates for SPAMI list (Joint Management Action of the European Community with the United Nations Environment Programme and Mediterranean Action Plan, 2010). The study area - Graham Bank, Nereo Bank and Pantelleria Vecchia Bank - falls into the PCA called Northern Strait of Sicily (Central Mediterranean Sea). These banks are also included in the ‘Sicilian Channel’ Ecologically or Biologically Significant Marine Area (EBSA), recognized in 2014 by the Contracting Parties of the Convention on Biological Diversity (CBD) (COP 12 Decisions, 2014). The EBSAs are special areas in the ocean that serve important purposes to support the healthy functioning of oceans and the many services that it provides (Conference of the Parties to the

http://dx.doi.org/10.1016/j.marenvres.2017.09.005 0141-1136/© 2017 Elsevier Ltd. All rights reserved.

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Convention on Biological Diversity, 2008). In 2008, the ninth meeting of the CBD (COP9) adopted seven scientific criteria for identifying ecologically or biologically significant marine areas in need of protection in open-ocean waters and deep-sea habitats. Although in 2010, the CBD (COP10) noted that application of the EBSA criteria is a scientific and technical exercise and that it has no obligation to consider MPAs directly, however, this recognition represents the first step provided by CBD to include an area in 10% of the marine biomes preserved by 2020 (Aichi Target 11). Indeed, areas found to meet the criteria may require enhanced conservation and management measures, which can be achieved through a variety of means. The EBSA criteria is an open and evolving process that should be continued to allow ongoing improvement and updating, as improved scientific and technical information becomes available in each region (Conference of the Parties to the Convention on Biological Diversity, 2008). In order to progress toward the achievement of the Aichi Target 11, conservationists urged upon the identification of priority 'biodiversity hotspots', mainly in the EBSAs, for protection and sustainable management (United Nations Environment Programme and Mediterranean Action Plan, 2015; Myers et al., 2000). In 2015 during the second RAC/SPA consultation meeting for the neighboring countries of the open seas of the Sicily Channel/ Tunisian Plateau (April 2015, Sciacca, Italy) was pointed out the need to define specific hot spots of biodiversity within the Strait of Sicily, where develop SPAMIs in areas beyond national jurisdiction. The paper intends to demonstrate that Graham Bank, Nereo Bank and Pantelleria Vecchia Bank represent, in a wide and diversified EBSA area, hot spots of biodiversity, with distinct strengths and weaknesses. The study also demonstrated that these remote areas are under threat and for this reason, require a site-specific, spatially explicit conservation policy. The Graham Bank, Nereo Bank and Pantelleria Vecchia Bank can represent eligible points for the institution of efficient and realistic area-based management measures, able to guarantee their protection and sustainable use. The Strait of Sicily represents a point of connection between the Western and Eastern Mediterranean basin. It is a vast physiographic and tectonic structure among Italy, Tunisia and Malta. The Strait comprises the eastern sill with a maximum depth of about 540 m and the western sill, which have a maximum depth of 530 m sloping into the central basin with deep trenches more than 1700 m deep, oriented northwest-southeast (Boccaletti et al., 1987; Cello,  1987; Civile et al., 2010; Reuther and Eisbacher, 1985; Spano et al., 2013). The Strait of Sicily geomorphology is characterized by the presence of Banks, extensive offshore shallow waters of different origin and morphology (volcanoes and sedimentary rocks) (Civile, 2015; Colantoni, 1985; Falzone et al, 2009). The complex bathymetry of the Strait of Sicily influences on the mesoscale oceanography, characterized by filaments, meanders and eddies, that along the shelf edge of the Banks can cause upwelling, able to locally increase biological productivity. Moreover, the Strait of Sicily plays an important role as nursery, spawning and/or recruitment areas for many fishing target species (Bo et al., 2008; Fiorentino et al., 2003, 2004, 2008, 2011; Freiwald and Taviani, 2009; Gancitano et al., 2008, 2011; Garofalo et al., 2008;  et al., 2013; Gristina et al., 2013; Ragonese et al., 2009; Spano Zibrowius and Taviani, 2005). It's worthy to note the recent detection of submarine hydrothermal activity, nearby some banks of late volcanism origin, relevant not only from a geological point of view but also for the related biological aspects (Bosman et al., 2008; Esposito et al., 2015; Falzone et al., 2009; Giacobbe et al., 2011). The results of this paper may represent a support system for international decision makers involved in protection and valorization of the Mediterranean open sea areas. The applied area-specific,

semi-quantitative scoring methodology was based on Taranto et al. (2012) method: the Ecosystem Evaluation Framework for global Seamount conservation and management. The framework, initially elaborated by Pitcher and Bulman (2007) and Pitcher et al. (2007, 2010), was developed within the conservation part of the Seamount Ecosystem Evaluation Framework, SEEF, in order to locate potential ecologically or biologically significant seamount areas and evaluate its main threats, based on the best information currently available. The SEEF can provide an intuitive form of systematizing and displaying of information, and can supply a platform both to characterize peculiarities of seamounts and identify knowledge gaps (Kvile et al., 2014). The data set utilized in this study came from an accurate literature review and the preliminary results of two scientific surveys carried out in 2014 and 2015, by the Italian National Institute for Environmental Protection and Research (ISPRA) in the frame of the project ‘Regional Observatory of marine and terrestrial Biodiversity of the Sicilian Region (ORBS). This method could be a valid support to pinpoint the priority Mediterranean banks for conservation management. 2. Materials and methods 2.1. Study area The paper is focused on three banks located in international water in the Strait of Sicily (United Nations Convention on the Law of the Sea, 1982), Central Mediterranean Sea: Graham Bank, Nereo Bank and Pantelleria Vecchia Bank. In Fig. 1 the main banks of the Strait of Sicily were represented, following the official localization of the Italian Navy Hydrographic Institute; the square points indicate the investigated banks. In this paper the term ‘bank’ is used to indicate morphological highs in open sea. Following Staudigel et al. (2010), seamounts will be also included, defined as: “any geographically isolated topographic feature on the seafloor taller than 100 m, including ones whose summit regions may temporarily emerge above sea level, but not including features that are located on continental shelves or that are part of other major landmasses”. The Graham Bank is composed by numerous volcanic edifices, mainly oriented NW-SE, such as the ephemeral Ferdinandea Island, located about 30 nautical miles from Pantelleria Island and 16 nautical miles from Sciacca. The volcanic cones are all well developed and vary widely both in size and depth, ranging from 9 m b.s.l. (ephemeral Ferdinandea Island) and 250 m b.s.l. (Falzone et al., 2009; Rovere and Wurtz, 2015). The Nereo Bank represents one of the numerous shallows spotting the Adventure Plateau, the wide and flat continental platform of carbonatic origin in the north-western sector of the Strait of Sicily (Colantoni et al., 1985). This morphological high is located about 19 nautical miles from the south-west coast of Sicily. The Bank is composed of three main parallel NE-trending minor shoals separated by narrow channels. In this study, the northern main ridge was investigated; it is about 3.7 km long and 3.5 km wide, ranging from about 30 m to 60 m of depth (Civile et al., 2015). The Pantelleria Vecchia Bank, along with Nereo Bank and many other morphological highs, compose the Adventure Archipelago within the Adventure plateau. This Bank is located 20 nautical miles north of Pantelleria Island. It is composed of two main shoals, ranging from 16 to 24 m b.s.l., and a number of smaller isolated bathymetric highs (Lodolo and Ben-Avraham, 2015). 2.2. Ecosystem evaluation framework In order to demonstrate that the investigated banks represent

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Fig. 1. Banks of the Strait of Sicily following the official delimitation of the Italian Navy Hydrographic Institute. The square points indicate the investigated Banks. Close to northwestern limit are located two other famous shallows: Talbot and Skerki.

hot spot of biodiversity under threat, a multidisciplinary approach was adopted, referring to both the methodology used and the issues investigated (biological/ecological traits, threats and pressures). The ecosystem evaluation framework, developed by Taranto et al. (2012), was applied and adapted to Mediterranean environment. In the present study this method was used and implemented to evaluate the Ecological and Biological Value (EBV) of Graham, Nereo and Pantelleria Vecchia Banks and the pressures and threats which they are subjected to. This method consists in a semi-quantitative scoring of an individual seamount likelihood to be an EBSA and the main threats that is exposed to. The model is a deepening of the methodology adopted in 2008 by the CBD COP9 for identifying EBSAs, based on seven criteria: C1Uniqueness or rarity; C2-Special importance for life-history stages of species; C3-Importance for threatened, endangered or declining species and/or habitats; C4-Vulnerability, fragility, sensitivity, or slow recovery; C5-Biological productivity; C6-Biological diversity; C7-Naturalness. The model includes four steps (Fig. 2). The first three steps, in turn, split in two, including the methodology to assess the bank Ecological and Biological Value (EBV steps) and the main threats posed to an individual bank (Threat steps). 2.2.1. EBV and threat indicators dataset Dataset for banks ecosystem evaluation was obtained by reviewing the existing literature in various fields of natural sciences, from 1970 to present days. In total, 188 scientific works concerning the Strait of Sicily were collected and examined. The acquired references were organized in a database. Each record contained information related to:  Bibliographic resources: scientific publications, grey literature (public bodies technical reports, NGO reports, white papers, thesis etc.);  Origin and nature of the collected data: scientific surveys, model application, undisclosed data, etc.;

Fig. 2. Summary of the Ecosystem evaluation framework modified from Taranto et al. (2012). The method includes four steps; the first three steps, in turn, split in two, including the methodology developed to assess the Ecological and Biological Value of banks (EBV) and the methodology followed to assess the main threats posed to an individual bank (Threats). The final step represents the plots of the bank EBV scores versus threat scores: on the left the bank EBV portfolio plot based on EBV scores and threat scores; on the right a radar plot reporting the components of the bank ecosystem contributing to the EBV score and its threat status.

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 Presence/absence of data on most important abiotic and biotic factors (geomorphology, oceanography, protected species, protected habitats, alien species, human impacts, etc.);  Presence/absence of data on EBV indicators and Threat indicators;  Type of information or descriptions: complete quantitative information, incomplete quantitative information, qualitative descriptions;  Data quality value (low, medium, high, not scored) In order to facilitate the consultation and analysis of the bibliographic resources, coded fields and keywords were integrated in the database, providing easy query and access to data. Another important source of data derives from two research survey was carried out in JuneeJuly 2014 and June 2015 by the Italian National Institute for Environmental Protection and Research (ISPRA) on board of the R/V Astrea to collect data on megabenthic and benthopelagic biodiversity of the Graham, Nereo, and Pantelleria Vecchia banks. The species and habitat diversity was mainly studied, on a qualitative level, by visual census carried out with remotely operated vehicle (ROV). A digital archive of 14 HD videos of bottom imagery and 1630 HD images was created.

(Council of Europe, 1979, 1992; United Nations Environment Programme, 1973; United Nation Environment Programme and Mediterranean Action Plan, 1995). ‘Coralligenous’, ‘Semi-dark caves’ and ‘Shelf-edge rock’ were €rl facies, association with introduced as C3, C4, C6 indicators; mae €rl/Rodholithes’) and facies ‘Soft muds with Funirhodolithes (‘Mae culina quadrangularis’ as C3, C4 indicators. Indeed, these environments play an important ecological role in the Mediterranean Sea and are seriously threatened by human activities (Bo et al., 2012; Giaccone, 2007; Giaccone et al., 1972; Relini and Giaccone, 2009). The ‘Shelf-edge rock’ indicator is characterized by the presence of cnidaria; amongst gorgonians, Callogorgia verticillata, Paramuricea clavata, Bebryce mollis, Villogorgia bebrycoides, Corallium rubrum, Leptogorgia sarmentosa, and amongst antipatharians, Antipathella subpinnata, Antipathes dichotoma and Parantipathes larix (Bo et al., 2012). The cnidaria included in the ‘Cold water corals’ indicator are the ones reported in Freiwald and Taviani (2009) and in Zibrowius and Taviani (2005): Lophelia pertusa, Madrepora oculata. An EBV score was attributed to each bank, related to the number of indicators detected and their weight (Step 3). The EBV was calculated as follows:

EBV ¼ 1 þ 2.2.2. Bank EBV: criteria, indicators and scoring procedure A general evaluation of the Ecological and Biological Value (EBV) of each bank, following the EBSA criteria was carried out (Step 1). Bank-specific EBV indicators were developed to improve the use of CBD EBSA criteria in identifying those banks more likely to be suitable for protection (Step 2) (Table 1). In this study, considering the C2 criterion (special importance for life-history of species), the indicator ‘Aggregating bank species’ was used and can be defined as: fishes, cephalopods and crustaceans which, in one or more stages of their life-history, form large aggregations around these features and comprise the main target for fisheries on banks (modified definition from Pitcher et al. (2008)) As far as C3 criterion is concerned, species and habitats were considered threatened, endangered, or declining if listed in the IUCN red list (Global, Mediterranean and Italian) (International Union for Conservation of Nature , 2015; Italian Committee of International Union for Conservation of Nature , 2016) and/or in the list of species and habitats protected or whose exploitation is regulated in accordance with the main international conventions and EU directives: CITES-Washington Convention, Berne Convention, Habitat Directive, SPA/BD Protocol of Barcelona Convention

P W P EBV bank indicator  4 WEBV indicator

(1)

Where SWEBV bank indicator is the sum of weights of indicators discovered on the bank (as number of criteria which indicator is able to verify) (Table 1) and SWEBV indicator is the sum of weights of all indicators. The ratio represent a weighted average of the EBV indicators. The Ecological and Biological Value ranging from 1, minimun EBV score - no indicators were detected, to 5, maximun EBV score all indicators were detected. Two value categories were considered: low EBV, scores 3 and high EBV, scores >3.

2.2.3. Bank threats and pressure: criteria, indicators and scoring procedure A general evaluation of threats and pressures posed to each bank was carried out (Step 1). In this study, fishing, debris, invasive alien species (IAS) and mining were considered as the major pressures and threats to the banks ecosystems (Step 2) (Table 2). These indicators are also included in Table 2 of Annex III of the Marine Strategy Framework Directive (2008/56/EC) (European Parliament and Council, 2008),

Table 1 The indicators used to identify bank EBV related to CBD EBSA criteria with their different ecological groups and weight (modified from Taranto et al. (2012)). Ecological group

Bank EBV Indicator

EBSA Criteriaa

Weight

Benthic

Hydrothermal vents Macrophytes Cold water corals Sponge aggregations Coralligenousb Semi-dark cavesb €rl/Rhodolithesb Mae Shelf-edge rockb Bathial muds with Funiculina quadrangularisb Threatened bottom sharks and fishes Aggregating bank speciesb Threatened air-breathing visitors OR air-breathing visitors Threatened visiting large pelagics OR visiting large pelagics Naturalness Depth

C1, C1, C3, C3, C3, C3, C3, C3, C3, C3 C2, C2, C2, C7 C5

3 3 3 3 3 3 2 3 2 1 2 2 OR 1 2 OR 1 1 1

Benthopelagic Benthopelagic/Pelagic Pelagic Historical Geological

C4, C5, C4, C4, C4, C4, C4 C4, C4 C4 C3 C3

C5 C6 C6 C6 C6 C6 C6

a CBD EBSA criteria: C1-Uniqueness or rarity; C2-Special importance for life-history stages of species; C3-Importance for threatened, endangered or declining species and/or habitats; C4-Vulnerability, fragility, sensitivity, or slow recovery; C5-Biological productivity; C6-Biological diversity; C7-Naturalness. b New indicators introduced respect to Taranto et al. (2012).

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Table 2 Impact of pressures (fishing activities, debris, invasive alien species) and threats (mining) on bank ecosystems. A scoring system for threats on ecological groups (benthic, benthopelagic, pelagic) are shown (modified from Taranto et al. (2012). Threats/Pressurea

Fishing gears Gillnet - bottom Hook and line Longline - bottom Longline - pelagic Pots and traps Purse seine Trawl - bottom Trawl - midwater Debrisb General litter Ghost gears Invasive alien speciesb Caulerpa cylindracea Caulerpa taxifolia Fistularia commersonii Saurida lessepsianus Siganus luridus Mining a b

Benthic

Benthopelagic

Pelagic

Physical habitat

Cold water corals, Sponge meadows

Groundfish

Large pelagics

Air-breathing

2 1 2 1 2 1 5 1

2 1 2 1 1 1 5 2

3 3 4 1 2 1 5 4

1 2 1 5 1 4 1 3

1 2 2 5 1 4 2 2

2 2

3 3

2 3

3 1

3 1

3 3 1 1 3 5

1 1 1 1 1 5

2 2 2 3 1 5

1 1 1 1 1 1

1 1 1 1 1 2

The impacts are defined as: 1, very low; 2, low; 3, medium; 4, high; and 5, very high. New threats/pressures introduced respect to Taranto et al. (2012).

where pressures and impacts interfering with the achievement of Good Environmental Status of marine waters of the Member States are reported. Fishing is identified both as a physical damage to the seabed, for the abrasion caused by some tools, and as a biological perturbation, for the selective extraction of species; debris is listed within other physical disturbance; alien species in biological perturbations; mining in physical damage. The main fishing gears used in the Strait of Sicily, from the infralittoral to the epybathial zone (Fiorentino et al., 2011), were chosen as fishing indicators. Debris is referred as a solid and persistent material of human origin either discarded or abandoned in the marine and coastal environment (Rees and Pond, 1995) able to interfere with life, prevent the gas exchange and release pollutions (Angiolillo et al., 2015; UNEP MAP/MED POL, 2009). In this paper benthic debris was taken in consideration, divided in general litter and ghost gears. The former includes plastic, metal and any other land and marine-based items discarded into the sea; the latter only the marine-based litter from commercial and recreational fishing. Invasive Alien species (IAS) can cause serious adverse impact on biodiversity and related ecosystem services (Council of Europe, 1992; European Parliament and Council, 2008, 2014; United Nation Environment Programme and Mediterranean Action Plan, 1995). Five species were selected as IAS indicators: Caulerpa cylindracea, Caulerpa taxifolia, Siganus luridus, Saurida lessepsianus (previously misidentified as S. undosquamis), Fistularia commersonii. They are included in the list of ‘100 Worst Invasive Species’ in the Mediterranean Sea (Streftaris and Zenetos, 2006) and detected in the Strait of Sicily close to the studied banks and/or with high affinity with the habitats of these banks. The alien algae Caulerpa cylindracea and Caulerpa taxifolia are characterized by rapid spread, high growth rate and ability to form dense meadows leading to reduction of species richness of native hard substrate algae by 25e55%, and, under certain conditions, outcompetes Posidonia oceanica and Cymodocea nodosa (Galil, 2007). The rabbit fish Siganus luridus is considered one of lessepsian species with greater expansion happened in much of the Mediterranean basin. It is an herbivorous fish and competes with native species (such Sarpa salpa); furthermore its feeding causes significant impact on the structure of the local algal community (Galil, 2007). This invasive

alien species may have profound impacts on native communities in the Mediterranean infralittoral zone (Giakoumi, 2014) and its presence on the banks could damage phisycal habitat and groundfish associated. Saurida lessepsianus, characterized by a rapid and massive spread, is a voracious predator, mainly piscivourous, competes with native species (e.g. Merluccius merluccius) and can even alter the biodiversity of an area, particularly the groundfish. The bluespotted cornet fish Fistularia commersoni entered the western Mediterranean basin in 2003 and in short time colonized all the Mediterranean (Castriota et al., 2014, and literature therein). F. commersonii is a fast-growing species and a higher order carnivore, almost exclusively piscivorous, with preys items ranging from bottom-dwelling fish and pelagic fish that shoal in the water column (Castriota et al., 2014; Psomadakis et al., 2009). These biological and ecological characteristics make the species a strong competitor for native species, such as groundfish on the bank. Although hydrocarbons and minerals research and exploitation activities have not been in progress on the investigated banks yet, mining activities is likely to pose a serious threat to bank ecosystems and was therefore considered as a threat (Halfar and Fujita, 2007; Halpern et al., 2008; He et al., 2011; Italian Ministry of Economic Development, 2016). A threat score (TS) was attributed to each bank (Step 3), as the average of the maximum impacts posed to the different ecological groups depending on the threat indicators detected and their impact on each ecological groups (benthic, benthopelagic, pelagic). The score ranging from 1 (low impact on ecological group) to 5 (high impact on ecological group) (Table 2). Three threat likelihood categories were considered: (TS) ¼ 1 e none impact; 1 < TS  3 e bank exposed to low impact; TS > 3 e bank exposed to high impact.

2.2.4. Bank EBV and threat data uncertainty index The EBV and Threat scoring procedure included the calculation of the Data Uncertainty index (DUEBV and DUTS respectively), proportional to data availability and quality. DU value ranges from 0 (low uncertainty) to approaching 2 (high uncertainty). DU is the sum of the Data Quality (DQ) index and the Data Deficiency (DD) index referred to an individual bank, as follows:

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Table 3 EBV indicators and EBV scores related to the Banks investigated. According to Taranto et al. (2012), the presence (1) or absence (0) of the EBV indicators is indicated as P/A. Indicators with no information available are marked as Data Deficient (DDEBVind). Indicator Data Quality (DQEBVind) is shown as: H ¼ high; M ¼ medium; L ¼ low. At bottom, bank EBV score, EBV likelihood category and Data Uncertainty (DUbankEBVscore) are reported for each bank, as well as the DUbankEBVscore components (DQbankEBVscore, DDbankEBVscore). Threatened air-breathing/air-breathing visitors and threatened visiting-pelagics/visiting-pelagics are mutual exclusive and therefore only one will be scored while the other will be empty (- ()). EBV indicator

Hydrothermal vents Macrophytes Cold water corals Sponge aggregations Coralligenous Semi-dark caves €rl/Rhodolithes Mae Shelf-edge rock Soft bathyal muds with Funiculina quadrangularis Threatened bottom fish or sharks Aggregating seamount species Threatened air-breathing visitors Air-breathing visitors Threatened visiting pelagics Visiting pelagics Naturallness Depth Bank EBV score EBV likelihood category DQbankEBVscore DDbankEBVscore DUbankEBVscore

Graham

Nereo

P/A (DQEBVind)

P/A (DQEBVind)

P/A (DQEBVind)

1 (L) 1 (M) 1 (L) 1 (L) 1 (L) 1 (H) 1 (L) 1 (H) 1 (H) 1 (L) 1 (L) 1 (L) - () 1 (L) - () 1 (L) 1 (H) 5.00 High 0.68 0.00 0.68

0 (H) 1 (L) 0 (H) 1 (L) 1 (L) 0 (L) 1 (L) 0 (H) 0 (H) 1 (M) 1 (L) 1 (L) - () 1 (L) - () 1 (L) 1 (H) 3.35 High 0.60 0.00 0.60

0 (H) 1 (M) 0 (H) 1 (L) 1 (L) 1 (H) 1 (L) 0 (H) 0 (H) 1 (L) 1 (L) 1 (L) - () 1 (L) - () 1 (L) 1 (H) 3.71 High 0.55 0.00 0.55

Table 4 Threat indicators and threat scores related to the investigated Banks. According to Taranto et al. (2012), the presence (1) or absence (0) of the Threat indicators is indicated as P/A. Indicators with no information available are marked as Data Deficient (DDTSind). Indicator Data Quality (DQTSind) is shown as: H ¼ high; M ¼ medium; L ¼ low. At bottom, mean threat score, threat category and Data Uncertainty (DUbankTSscore) are reported for each bank, as well as the DU components (DQbankTSscore, and DDbankTSscore). Threats/Pressure

Gillnet- bottom Hook and line Longline - bottom Longline - pelagic Pots and traps Purse seine Trawl - bottom Trawl - midwater General litter Ghost gears Caulerpa cylindracea Caulerpa taxifolia Fistularia commersonii Saurida lessepsianus Siganus luridus Mining Mean threat score Threat category DQbankTSscore DD bankTSscore DU bankTSscore

DUðEBV

or TSÞ

Graham

Nereo

P/A (DQTSind)

P/A (DQTSind)

P/A (DQTSind)

1 (L) DDind DDind DDind DDind DDind 1 (L) DDind 1 (H) 1 (H) 1 (L) 1 (L) 1 (L) 1 (L) 1 (L) 1 (L) 4.20 High 0.80 0.38 1.18

1 (L) DDind DDind DDind DDind 1 (H) 1 (L) DDind 1 (H) 1 (H) 1 (H) 1 (L) 1 (L) 1 (L) 1 (L) 1 (L) 4.60 High 0.73 0.31 1.04

1 (L) DDind DDind DDind DDind DDind 1 (L) DDind DDind 1 (H) 1 (H) 1 (L) 1 (L) 1 (L) 1 (L) 1 (L) 3.60 High 0.87 0.44 1.31

¼ DQðEBV

or TSÞ

þ DDðEBV

or TSÞ

Pantelleria Vecchia

(2)

P or TSÞ

¼

DQind Nind

P DDðEBV

or TSÞ

¼

DDind Nind

(4)

DQind is the Data quality index assigned to EBV or Threat indicator data collection and took into consideration the origin and nature of information and DDind indicates the absence of information about an indicator on a specific bank. DQind was divided into three classes (modified respect to Taranto et al. (2012) as follows:  High (scored as 0) - Rigorous scientific surveys: quantitative data or qualitative data, if in great detail, strictly referred to a specific bank;  Medium (scored as 0,5) - Rigorous scientific surveys: diachronic analysis of minimum 10 years (including models but only if statistically supported), validated in the literature, with incomplete quantitative information and/or qualitative descriptions strictly focused on the Strait of Sicily, with clear data on a specific bank;  Low (scored as 1) - Undisclosed data: data referring to wide geographic areas (comparable ecosystem in the Mediterranean Sea), which do not specifically address banks, and/or information inferred from models, and/or data from different bank properties, or data not properly referenced.

where

DQðEBV

Pantelleria Vecchia

(3)

2.2.5. EBV versus threat plot and EBV/Threat versus ecological groups According to Taranto et al. (2012), EBV likelihood and threats for each bank were summarized and graphically compared (Fig. 2, Step 4) in order to highlight the bank classification into conservation categories (EBV versus Threat plot), and the contribution of different ecological groups to the EBV and threat score (EBV/Threat versus ecological groups). Four categories of EBV versus Threat scores were distinguished and visualized as different areas (Low EBV/Low Threat; High EBV/

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Fig. 3. Bank EBV portfolio plot based on EBV scores and threat scores for Nereo (circle point), Graham (rhombus point) and Pantelleria Vecchia (square point) banks. According to Taranto et al. (2012), the different color represents four portfolio categories. Dark area: low EBV - low threats exposure. Dark grey area: low EBV - high threats exposure. Light grey area: high EBV - low threats exposure. Blank area: high EBV - high threats exposure. Error bars represent the data uncertainty index (DU, see methods) proportional to data availability and quality.

Low Threat; Low EBV/high Threat, High EBV/high Threat). The Data Uncertainty index (DU) was visualized as error bars in the plot chart (Fig. 2 on the left). The contribution of different ecological groups (e.g. benthic, benthopelagic or pelagic) to the EBV score and threat score was visualized by radar plot. The EBV component was shown as proportion of attributes present (in a 0 to 5 scale) in each bank, while the threats were given by the maximum threat estimated for each component of the ecosystem. EBV/Threat shows the final EBV and Threat scores for each bank (Fig. 2 on the right). 3. Results 3.1. EBV and threat indicators data set Most of the studies collected (84%) concerned the whole area of the Strait of Sicily, whilst poor information was available on banks. Considering the EBV and Threat indicators (Tables 1 and 2) - the works were mainly focused on fishing (biological and ecological aspects of fishing target species, their exploitation and the employed gears) (65%), alien species (15%) and geological issues (hydrothermal vents, volcanism, geomorphology, etc.) (15%). On the contrary, works focused on banks biodiversity - mainly benthic biocenosis - and threats and pressures posed to it, were lacking. The literature review concerning the fishing activity shown that the Strait of Sicily is an important area for the high productivity of fishing resources, particularly groundfish, supplying an important fishing fleet trawling, located in the various ports of southern Sicily. The trawling represent the most important method of fishing; in any fishing ports there are also a number of smaller vessels operating artisanal fisheries. The trawl fishery conducted in the Strait of Sicily belongs to two types: a coastal trawling with multispecies catches (red mullet, hake, pink shrimp, squid, octopus, etc..) and oceangoing trawlers operating in international waters, having as target species pink shrimp, red shrimp and mullet (Fiorentino et al., 2011). Regarding the banks, the most relevant target species of trawling are pelagic fishes (hake), benthic/benthopelagic fishes (scorpionfish, mullet, seabream, rays, etc.), cephalopods (squid, octopus, cuttlefish, etc.), and decapod crustaceans (pink shrimp,

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red shrimp, norway lobster, etc.) (Fiorentino et al., 2011; Gancitano et al., 2012; Garofalo et al., 2003). In addition, mainly in the eastern sector of the Adventure Plateau, upwelling generates areas poor in diversity but with a high ecosystem productivity and stable areas of nursery, spawning and recruitment of many fishing target species (Fiorentino et al., 2003; 2004, 2008, 2011; Garofalo et al., 2007; 2008, 2010, 2011). Regarding mining activities, the Nereo Bank and Graham Bank fall into the so-called Area C, which is the Italian area open, in 1967, to the research and production of hydrocarbons in the Sea, extended in 2012 until the isobath of 200 m. Pantelleria Vecchia lies instead in the Area G, open to the research and production of hydrocarbons in the Sea in 1982, included between the 200 m depth contour and the limit of territorial waters (United Nations Convention on the Law of the Sea, 1982). The banks are not involved in oil and gas research and exploitation yet; however, in these areas oil companies continue to search for new deposits to increase oil and gas mining, proved by the several applications for exploration and research permits (Italian Ministry of Economic Development, 2015). Most of the data on bank EBV indicators came from the ‘ORBS Banchi 2014e2015’ research surveys. In particular, the following indicators were indentified (Fig. 5): ‘Hydrothermal vents’ (Fig. 5a), ‘Macrophytes’ (Fig. 5b), ‘Coralligenous’ (Fig. 5c), ‘Semi-dark caves’, €rl/Rhodolithes’ (Fig. 5d), ‘Shelf-edge rock’ (Fig. 5eef), ‘Soft ‘Mae bathial muds with Funiculina quadrangularis’, ‘Ghost gears’ (Fig. 5g), ‘Invasive alien species’ (Fig. 5h). 3.2. Ecosystem evaluation The EBV score for the Graham, Nereo and Pantelleria Vecchia banks was reported in Table 3. The indicators detected are shown with related Data Quality index (DQEBVind). At bottom, the bank EBV score, the EBV likelihood category, the Data Quality index (DQbankEBVscore), the Data Deficiency index (DDbankEBVscore) and the Data Uncertainty index (DU) for each bank are reported. In Table 4 the Threat score for the evaluated banks was reported; each indicator detected were shown with related Data Quality index (DQTSind) and Data Deficiency index (DDind). At bottom, the mean threat scores, the threat categories, the Data Quality index (DQbankTSscore), the Data Deficiency index (DDbankTSscore) and the Data Uncertainty index (DUbankTSscore) were reported. The Graham Bank is included in the high EBV category, with the EBV score of 5.00 ± 0.68, it has the maximum score as all the indicators are present. The Data Uncertainty of 0.68 shows that the factors were scored with quite high data quality. All the indicators are present generally with a low DQEBVind excepting ‘Semi-dark caves’, ‘Shelf-edge rock’, ‘Soft bathyal muds with Funiculina quadrangularis’ and ‘Depth’, that are present with a high value of DQEBVind, and ‘Macrophytes’ present with a medium DQEBVind. The Bank is included in the high threat category as well (bank exposed to high impact), with the mean threat score of 4.20 ± 1.18. The Data Uncertainty of 1.18 shows that the factors were scored with middle data quality. As regard fishing gears, 2 out of 8 indicators are present (‘gillnet-bottom’ and ‘trawl-bottom’) with low DQTSind. ‘General litter’ and ‘Ghost gears’ are present with high value of DQTSind. The Nereo Bank is included in the high EBV category, with the EBV score of 3.35 ± 0.60. The Data Uncertainty of 0.60 shows that the factors were scored with quite high data quality. Ten out of 15 indicators are present, lacking ‘Hydrothermal vents’, ‘Cold water corals’, ‘Semi-dark caves’, ‘Shelf-edge rock’ and ‘Soft bathyal muds with Funiculina quadrangularis’. The DQEBVind is generally low excepting ‘Depth’, that is present with a high value of DQEBVind, and ‘Threatened bottom fish or sharks’ with a medium DQEBVind.

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The Bank is included in the high Threat category as well, with the mean threat score of 4.60 ± 1.04. The Data Uncertainty of 1.04 shows that the factors were scored with middle data quality. As regard fishing gears, 3 out of 8 indicators are present (‘Gillnetbottom’, ‘Purse seine’ and ‘Trawl-bottom’) with generally low DQTSind. ‘General litter’, ‘Ghost gears’ and, among IAS indicator, Caulerpa cylindracea, are present with high value of DQTSind. The Pantelleria Vecchia Bank is included in the high EBV category, with the EBV score of 3.71 ± 0.55. Also for this bank, the Data Uncertainty of 0.55 shows that the factors were scored with quite high data quality. Eleven out of 15 indicators are present, lacking ‘Hydrothermal vents’, ‘Cold water corals’, ‘Shelf-edge rock’, and ‘Soft bathial muds with Funiculina quadrangularis’. Among found indicators, the DQEBVind is generally low excepting ‘Depth ’ and ‘Semi-dark caves’, that are present with a high value of DQEBVind and ‘Microphytes’ with a medium DQ(ind). The Bank is included in the high Threat category as well, with the mean threat score of 3.60 ± 1.31. The Data Uncertainty of 1.31 shows that the factors were scored with middle data quality. As regard fishing gears, 2 out of 8 indicators are present (‘Gillnetbottom’ and ‘Trawl-bottom’) with low DQTSind. ‘Ghost gears’ and, among IAS indicator, Caulerpa cylindracea, are present with high value of DQTSind. In Fig. 3 the EBV versus Threat portfolio plot was reported. All the banks were included in the high EBV/high threat category (blank area). The Data Uncertainty index (DU), visualized as error bars, indicate that the three banks always fall into the high EBV category. The Pantelleria Vecchia Bank can possibly belong to high EBV/low threat category, corresponding to light grey area, and the Nereo Bank can possibly belong to Low EBV/High threat category, corresponding to dark grey area. Radar plots in Fig. 4 show that all the components of bank ecosystem - benthic, benthopelagic and pelagic ecological groups contribute to the final EBV score and have an EBV score ranging from 2.2 to 5. In all three banks, benthic and benthopelagic ecological groups were more exposed to threats (Threat score ¼ 5) due to the high score attributed to the trawl-bottom fishing gear (Table 2). On the Graham Bank all the components show the maximum EBV. On the Nereo and Pantelleria Vecchia banks the pelagic and benthopelagic components show the highest ecological and biological value; the benthic components have a value lower than 3 due to the lack of 5 indicators on the Nereo Bank and 4 indicators on the Pantelleria Vecchia Bank (Table 4).

4. Discussion The Convention on Biological Diversity (CBD) leads the creation of a network of Marine Protected Areas (MPAs), that should include a full range of examples across biogeographic regions, as defined by Global Open Oceans and Deep Seabed biogeographic classification (Briones et al., 2009). Special regard is to be given to the creation of MPAs in the open seas, to date the least protected areas in the oceans (United Nations Environment Programme and Mediterranean Action Plan, 2015). Currently, the Pelagos Sanctuary (France, Italy, Monaco) is the only protected area (United Nation Environment Programme and Mediterranean Action Plan, 1995, United Nations Environment Programme and Mediterranean Action Plan, 2015) covering offshore habitat in the Mediterranean Sea. The Strait of Sicily in the Central Mediterranean Sea is a very

Fig. 4. Components of the Graham, Nereo, and Pantelleria Banks ecosystem contributing to the EBV score and its threat status. Radar plots for individual bank showing

what parts of the ecosystems (benthic, benthopelagic and pelagic) are contributing to the EBV score (dark grey area) or being threatened by pressures and threats (light grey area). EBV/Threat shows the final EBV and Threat score for each bank (Tables 3 and 4).

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Fig. 5. ROV images related to some of the indicators identified during the ‘ORBS Banchi 2014e2015’ research surveys: (a) hydrothermal vents: gas emission (foreground) and whitish mineralization (background) on the Graham Bank; (b) macrophytes: Laminaria rodriguezii population on the Nereo Bank; (c) coralligenous: facies with Eunicella singularis on €rl/rhodolithes: association with rhodolithes on the Pantelleria Bank; (e) shelf-edge rock and ghost gears: Callogorgia verticillata with epibenthic ophiuroid the Nereo Bank; (d) mae and longlines on the Graham Bank; (f) shelf-edge rock: Corallium rubrum on the Graham Bank; (g) ghost gears: gillnet still fishing with bioconcretions on the Graham Bank; (h) invasive alien species: Caulerpa cylindracea, green algae on the Pantelleria Vecchia Bank. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

complex and articulated biogeographic area; one of a few sectors in the world with upper bathyal depth zones (Briones et al., 2009) in the open seas, including an extensive bank system. The whole Strait has been recently considered a relevant area of conservation concern; it was included in the twelve priority conservation areas likely to contain candidate sites for SPAMIs and listed in the EBSAs. This paper demonstrates that the Graham Bank, Nereo Bank and Pantelleria Vecchia Bank in the Strait of Sicily, although barely investigated yet, represent hot spot of biodiversity in open sea, playing a key role in sustaining the pelagic and benthic production in the Strait of Sicily. The banks show specific characteristics, largely different from the surrounding deep sea area of the Strait of Sicily;

it is of great importance to take in consideration their peculiarities to foster site-specific and spatially explicit management policy coming from International agreements. The conservation actions should be follow an ecosystem based management approach, able to integrate the preservation of undisturbed areas, the restoration of damaged ecosystems and the respect of the socio-economic background. Although the banks fall in the high EBV/high Threat category, they are also characterized by wide pristine areas to be protected by an appropriate monitoring and regulation of fishing activity, alien species spread, presence and diffusion of general litter and ghost gears, and mining activity. The semi-quantitative scoring procedure of Taranto et al. (2012) was adapted to the specific traits of the banks at issue by means

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“Ecological and Biological Value” and “threats/pressures” indicators implementations. This methodology allowed to demonstrate in a simple and practical manner: - biological and ecological value of the banks by presence/absence of indicators related to CBD EBSA criteria; - pressures posed to the banks and threats in the near future; - current gap of knowledge that needs further investigations. This method could be also used to assess the biological and ecological value of other Mediterranean banks and set priorities in their conservation. The confidence about the ecological and biological valuation is quite high; in fact, ecosystem data are widely available, despite their low quality due to the considerable lack of bank-specific knowledge. Less information is available on threats and pressures posed to bank communities due to the absence or low quality of the existing data. As confirmed by several studies, fishing activity is the most important human pressures posed to the banks, that represent aggregating area for many fish species; most of them are fundamental target for fishery and currently are in a condition of overfishing (Fiorentino et al., 2011; Gancitano et al., 2011). Future surveys in these banks should be focused on species and ecosystem biodiversity to map the pristine areas and damaged areas. In detail, referring to hydrothermal vents, at the light of the available data, they result absent on the Nereo Bank, but it is only one of the numerous shallows of the Adventure Plateau, including also seamounts such as Galatea, Tetide and Anfitrite, whose hydrothermal activity needs to be deepened. Moreover, no information is available on vents communities on the Graham Bank; as observed in similar environments in the Aeolian Islands (Esposito et al., 2015; Giacobbe et al., 2011), the hydrothermal vents can host peculiar benthic communities able to exploit the gas emissions as source of energy thanks to procariotic organisms. Other indicators, like ‘Macrophytes’, ‘Coralligenous’, ‘Semi-dark caves’, €rl/Rhodolithes'and ‘Shelf-edge rock’, represent benthic com‘Mae munities with high level of biodiversity, found in good condition of preservation in different zones of the banks. Said biocenosis deserve in these pristine areas further taxonomic, structural and compositional studies, considering their rarity along the coast brought about human activities and their wide distribution on all three Banks. On the Nereo and Pantelleria Vecchia banks the lower ecological an biological value respect to the Graham Bank is due to their lower depth that prevent the development of the habitats: shelf-edge rock, cold water corals and soft bathyal muds with Funiculina quadranguralis. On the Graham Bank it would be interesting to explore the bathyal substrates below the isobath of 250 m, to investigate the presence of the cold water corals and sponge aggregations. Site-specific studies on commercial and recreational fishery are also necessary, focused on fishing gears, fishing effort and catching, as well as on ghost gears and general litter. This information is mainly lacking on the Pantelleria Vecchia Bank. Ghost gears cause a significant and persistent impact on different ecological groups; they may cause damage to benthic habitats and species, for example, abrading, entangling and breaking branched organisms, that, weakened, are more easily overgrown and suffocated by opportunistic epibiontic species. Moreover, they may continue to catch a large spectrum of organisms (Bo et al., 2014). Further investigations should also include the analysis of invasive alien species. Currently, the ROV survey shown the presence of Caulerpa cylindracea detected on the Nereo and Pantelleria Vecchia banks (Fig. 5h). Although the other IAS have not been recorded on

the banks yet, their invasive capacity and their frequent records in the Straits of Sicily leave hypothesize their presence or imminent arrival on the banks. For this reason it would be appropriate a continuous monitoring of the banks focused on this issue, in particular on the IAS impacts posed to physical habitat and groundfish. In conclusion, although mining activities have not been affecting the investigated banks yet, the interest of the oil companies is getting stronger against these offshore shallow areas, representing a threat in the near future. These further studies would help the delimitation of marine protected areas, including the investigated banks and other ones of the Strait of Sicily with a high ecological and biological value under pressure. These hot spots of biodiversity could represent a network of MPAs in the open sea. The inclusion on the banks in a MPA, like a SPAMI, would encourage the identification of zones with different area-based management measures. An example of this management approach is suggested by Man and the Biosphere (MAB) Programme for the designation of UNESCO biosphere reserve. In said reserve the core area is devoted to long term protection with specific conservation objectives; in the buffer zone only activities compatible with the conservation objectives can take place; in the transition area sustainable resource management practices are promoted and developed. In order to protect the banks, the future challenges are to promote further scientific researches, strength international political collaboration and foster the involvement of local stakeholders and populations, as recommended in the Annex I of SPA/BD protocol, reporting the criteria for the choice of protected marine and coastal areas that could be included in the SPAMI list. Acknowledgments This paper is dedicated to Giovanni Bortoluzzi who attended, with passion, commitment and professionality, to the ‘ORBS Banchi 2014e2015’ research surveys, and who suddenly passed away in October 2015. We thank to the authors of the paper Taranto et al., 2012 for inspiring us this study. We thank to Pietro Battaglia, Silvana Campagnuolo, Luca Castriota, Mauro Sinopoli for participating to the ‘ORBS Banchi 2014e2015’ research surveys. This work was supported by D.R.A. Assessorato Territorio Ambiente Regione Siciliana; Asse 3 Linea di intervento 3.2.1.2 of POR FESR Sicilia 2007e2013 aimed to assess marine biodiversity in Sicily. References Angiolillo, M., di Lorenzo, B., Farcomeni, A., Bo, M., Bavestrello, G., Santangelo, G., Cau, A., Mastascusa, V., Cau, A., Sacco, F., Canese, S., 2015 Mar 15. Distribution and assessment of marine debris in the deep Tyrrhenian sea (NW Mediterranean sea, Italy). Mar. Pollut. Bull. 92 (1), 149e159. , N., Bavestrello, G., 2008 Jun 1. Antipathella subpinnata Bo, M., Tazioli, S., Spano (Antipatharia, Myriopathidae) in Italian seas. Italian J. Zoology 75 (2), 185e195. Bo, M., Canese, S., Spaggiari, C., Pusceddu, A., Bertolino, M., Angiolillo, M., Giusti, M., Loreto, M.F., Salvati, E., Greco, S., Bavestrello, G., 2012 Nov 21. Deep coral oases in the south Tyrrhenian sea. PloS one 7 (11). Bo, M., Bava, S., Canese, S., Angiolillo, M., Cattaneo-Vietti, R., Bavestrello, G., 2014. Fishing impact on deep Mediterranean rocky habitats as revealed by ROV investigation. Biol. Conserv. 171, 167e176. Boccaletti, M., Cello, G., Tortorici, L., 1987 Dec 31. Transtensional tectonics in the Sicily Channel. J. Struct. Geol. 9 (7), 869e876. Bosman, A., Calarco, M., Casalbore, D., Chiocci, F.L., Coltelli, M., Conte, A.M., Martorelli, E., Romagnoli, C., Sposato, A., 2008. Submarine volcanic features in the Pantelleria offshore revealed by high resolution swath bathymetry. Rendic Soc. Geol. Ital. 3, 128e129. Briones, E.E., Rice, J., Ardron, J., 2009. Global Open Oceans and Deep Seabed (GOODS) Biogeographic Classification. UNESCO, IOC, 54 pp. Castriota, L., Falautano, M., Battaglia, P., Oddo, A., Andaloro, F., 2014 Jan 31. New biological data on Fistularia commersonii in the central Mediterranean Sea. CYBIUM 38 (1), 15e21.

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