Abstract
An updated overview of the marine alien and cryptogenic species recorded in the Egadi Islands Marine Protected Area (Tyrrhenian Sea, Italy), based on relevant publications, grey literature and unpublished data, is presented and discussed. Altogether, 17 species (14 aliens and 3 cryptogenic) belonging to five taxa are present in the area: Rhodophyta (Antithamnionella elegans, Asparagopsis armata, Asparagopsis taxiformis, Bonnemaisonia hamifera, Botryocladia madagascariensis, Ceramium strobiliforme, Laurencia caduciramulosa, Lophocladia lallemandii, Neosiphonia harveyi, Womersleyella setacea), Chlorophyta (Caulerpa cylindracea and Caulerpa taxifolia), Mollusca (Aplysia dactylomela), Arthropoda (Percnon gibbesi) and Cordata (Fistularia commersonii, Kyphosus vaigiensis and Stephanolepis diaspros). The overall Mediterranean presence of one further taxon recorded from the area, Zygochlamys patagonica (Mollusca), is here confuted since recent findings of living specimens with certain data are missing. One loose valve of “Pinctada imbricata radiata (Mollusca)” was found in 2010 at Favignana, but we did not include it in the list of alien species, pending further finding of living or dead specimens. Unpublished distributional data are reported for some of these species, and their known distribution in the Aegadian Archipelago is mapped. Records of P. gibbesi (a conspicuous number of specimens) constitute the first for the archipelago. All the species included in the present paper were recorded after the Egadi Islands Marine Protected Area was established, with the first record dating back to 2000. This is presumably due to the recent increase in research programs on marine reserves. Finally, we provide the establishment status of all the recorded species updated to 2015, and discuss why unaided spread (whether alien or native) and/or transport-stowaway constitute the more plausible vectors of introduction.
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Introduction
Alien species are presently considered one of the most serious threats, after habitat destruction, to biodiversity and natural ecosystem functioning (Bax et al. 2003; Wallentinus and Nyberg 2007). Marine alien species may become invasive and have significant effects on the environment (biodiversity loss, habitat modifications and alterations in community structure), economy and human health (Galil 2007; Katsanevakis et al. 2014), raising serious concerns in the scientific community.
The Mediterranean Sea is an important hotspot of marine biodiversity, also for alien species, and it is one of the major areas severely affected by marine invasions, in terms of both the number of species and the rate of introduction (Coll et al. 2010; Lejeusne et al. 2010; Zenetos et al. 2012; Galil et al. 2015). The number of marine alien species reported so far ranges from more than 600 to nearly 1.000 (Zenetos et al. 2012; Galil and Goren 2014). The reported discrepancies in numbers are mostly due to difficulties in objectively assessing whether the spread of taxa is due to natural dispersal or to human activities. A conspicuous increase in the rate of introduction of marine alien species has been noticed during recent decades (Zenetos et al. 2010; Occhipinti-Ambrogi et al. 2011a, b; Katsanevakis et al. 2013), due to escape from confinement, transport-stowaway and corridor (Suez Canal) entries (categories according to the Convention on Biological Diversity: CBD 2014). Within the Mediterranean Sea, a relatively high number of marine alien species occur around the Italian peninsula (Occhipinti-Ambrogi et al. 2011a, b), and, in particular, Sicily and its surrounding islands are characterized by intense maritime traffic, including that related to fisheries and recreation (Occhipinti-Ambrogi et al. 2011a, b; Katsanevakis et al. 2014). These and other human activities fostering the introduction of marine alien species, have made the region vulnerable and susceptible to biological invasions (Bianchi 2007; Occhipinti-Ambrogi et al. 2011a, b; Katsanevakis et al. 2012), despite the high number of Marine Protected Areas (MPAs) already established. Even though MPAs have a strong potential for habitat and biodiversity conservation, they seem to be ineffective in protecting from biological invasions, and in some cases may enhance them (e.g. Byers 2005; Klinger et al. 2006; Burfeind et al. 2013). In fact, high numbers of visitors, increasing disturbance, vectors (e.g. boat anchors, SCUBA equipment, bilge water, hull fouling) and subsequent dispersal of propagules (Minchinton and Bertness 2003; West et al. 2007; Britton-Simmons and Abbott 2008; Burfeind et al. 2013) could promote the introduction of invasive species.
Since reliable and accessible information (inventories, databases, literature) on distribution and status, introduction vectors and impacts of marine alien species is crucial for planning effective management and conservation strategies, the aim of the present paper is to offer an updated overview on the marine alien and cryptogenic species from the Egadi Islands MPA (Aegadian archipelago, Tyrrhenian Sea, Italy), especially in order to provide a baseline report of the situation up to 2015, necessary for planning future research and activities within the MPA.
Materials and methods
Description of the area
The Egadi Islands MPA, the largest Italian MPA which was instituted in 1991, is a small archipelago located approximately 7–9 km from the western coast of Sicily (Italy, Tyrrhenian Sea). It is composed of three main islands (Favignana, Marettimo and Levanzo) and a few small islets (Galeotta, Galera, Preveto, Formica and Maraone) (Fig. 1).
Literature research and unpublished data
All the relevant publications and reports dealing with marine alien and cryptogenic species in the Egadi Islands MPA were searched and analysed. Unpublished data provided by the authors of the present paper were included, as well as personal communications provided by skilled citizen scientists. Sites of occurrence of marine alien and cryptogenic species are listed in Table 1, while detailed information on the records is reported in Table 2.
Three main mechanisms of introduction are recognized by the CBD (2014): importation of a commodity, arrival via a transport vector, or spread from a neighbouring region. The most plausible pathways of introduction in the Egadi Islands MPA were attributed according to the hierarchical pathway classification adopted by the CBD (2014). In particular, the following two categories were considered: (1) the transport-stowaway (S-T), which mostly “refers to the moving of live organisms attached to transporting vessels and associated equipment and media”, and (2) the unaided spread (US), which refers to the secondary dispersal of alien species from neighboring areas. However, since in our list we have also retained species which may turn out to be vagrants and not truly aliens, we have used this term cautiously, since unaided spread may possibly be nothing more than natural spread.
The establishment success of each species was determined on the basis of published and unpublished data. We considered species as casual (C) (here synonymous with non-established) when recorded only once on the basis of one or very few specimens, and as established (E) when the species was either established in the wild with free-living, self-maintaining and self-perpetuating populations, or recorded at least twice and spread over time and space.
Alien species definition
The definition of alien species (non-native, non-indigenous, exotic) used here follows the European Commission (EC 2008): “a species, subspecies or lower taxon, introduced outside its natural past or present distribution; includes any part, gametes, seeds, eggs, or propagules of such species that might survive and subsequently reproduce”. However, some species recently recorded from the Mediterranean cannot be described with certainty as native (therefore including vagrant, according to the EC definition of “alien species”) or alien, and may be cryptogenic (see Carlton 1996: a species that cannot be included with confidence among native nor among introduced ones).
So far, this term has been mostly used in defining circumtropical species or species with a disjoint distribution, and whose native range is still unknown or whose presence may be the result of past introductions not recorded in the literature (Carlton 2009). This term has also been applied to small, cryptic species that may have gone unnoticed for hundreds of years. In contrast, in some cases (e.g. large and/or obvious shallow water species), we are dealing with taxa clearly recorded for the Mediterranean relatively recently, excluding the possibility that their historical presence in the Mediterranean may have gone unnoticed, and whose vector of arrival in the Mediterranean is still unknown and may be due to natural spread or human activities. We also considered these species as “cryptogenic”, pending the possibility to include or exclude them from alien lists in the future.
Results and discussion
Altogether, 14 alien and 3 cryptogenic species have been recorded from the Egadi Islands MPA (some of them are shown in Fig. 2). Ten are Rhodophyta, two are Chlorophyta, one Mollusca, one Crustacea and three are Pisces. Another species reported from Favignana, Zygochlamys patagonica (King, 1832) [Repetto (1989) as Chlamys lischkei (Dunker, 1850)], was excluded. This species is still reported in some Mediterranean lists (e.g. Zenetos et al. 2004, 2010; Templado and Villanueva in Coll et al. 2010; Galil et al. 2016) due to three Mediterranean records (Gubbioli and Nofroni 1985; Repetto 1989; Crocetta and Renda 2008). However, since we are not sure if all Mediterranean records are based on discards in the field of dead specimens imported with shrimps (some presumably even with soft parts), or that specimens obtained “from fishermen” may refer to trawlings from the Atlantic by fleets based only in the Mediterranean Sea, we suggest the exclusion of this taxon from all Mediterranean lists until confirmed by recent findings of living specimens with certain distributional data. One loose valve of “Pinctada imbricata radiata (Leach, 1814)”, according to major databases (e.g. Bouchet 2015), was first found in the Egadi Islands MPA in 2010 at Favignana (P. Balistreri, unpublished data). We cannot say with certainty if the specimen lived where it was found, or if it was discarded in the area. Therefore, we did not include it in the list of alien species, pending further findings of living or dead specimens.
All records come from the three main islands only; there are no records from the small islets, presumably due to their limited coastlines and the few field studies carried out in these areas. The known distribution of the taxa included in the present review is reported in Table 2 and shown in Fig. 1 (see Table 1 for the site codes). Among them, the occurrence of Percnon gibbesi (H. Milne Edwards, 1853) constitutes the first confirmed record from the Egadi Islands MPA. The most plausible vectors of arrival in the Egadi Islands MPA and local establishment success are reported in Table 2.
Antithamnionella elegans (Berthold) J.H. Price & D.M. John, 1986
Status: ALIEN SPECIES
Remarks: first reported from the Mediterranean Sea prior to 1882 in the Gulf of Naples (Berthold 1882) as Antithamnion elegans Berthold, 1882. Transport-stowaway is considered the plausible pathway of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Levanzo (40 m depth) and Marettimo (0, 1 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Asparagopsis armata Harvey, 1855 complex
(Fig. 2a)
Status: ALIEN SPECIES
Remarks: originally described from western Australia, specimens from several biogeographic areas morphologically ascribed to Asparagopsis armata Harvey, 1855 belong to a complex of cryptic species (see Dijoux et al. 2014), and therefore we report them as “Asparagopsis armata Harvey, 1855 complex”. According to Dijoux et al. (2014), A. armata specimens from Europe fall within the same clade as South African and Tanzanian specimens, while another newly discovered clade is restricted to western Australia, Tasmania and New Zealand. Specimens belonging to this complex of species were first reported in the Mediterranean Sea in 1923, from the Algerian coast (Feldman and Feldman 1942), and their alien status in the Mediterranean area has been confirmed by the molecular studies of Andreakis et al. (2004, 2007).
Presence in the Egadi Islands MPA: the first report of specimens belonging to this complex of species from the Egadi Islands MPA dates back to 2001 (Catra et al. 2006). Specimens were found in several sites along the coasts of the three main islands. At Favignana, it was recorded from 0 to 30 m depth, at Levanzo from 0 to 40 m depth, and at Marettimo from 0 to 25 m depth. From 2006 onwards, the alga was recorded again at Favignana, mainly on rocks between 0.5 and 6 m depth (R. D’Agostaro, unpublished data; P. Balistreri, unpublished data). Both unaided spread or transport-stowaway may be plausible pathways of introduction for local specimens.
Asparagopsis taxiformis (Delile) Trevisan de Saint-Léon, 1845 complex
(Fig. 2b)
Status: ALIEN SPECIES
Remarks: Asparagopsis taxiformis (Delile) Trevisan de Saint-Léon, 1845 was originally described by Delile (1813) with Alexandria (Egypt, Mediterranean Sea) as type locality. Being mostly diffused in the Indo-Pacific, several authors considered it in the past as a Tethyan relict (Cormaci et al. 2004) or a pre-Lessepsian immigrant (Por 1978). However, recent molecular data showed that the A. taxiformis complex is composed of 5 different clades (type material, if existing, not yet barcoded), although the recent publication by Dijoux et al. (2014) did not resolve the taxonomic status of the known lineages. However, we here cautiously report it as a complex of species, also in agreement with previous studies by Andreakis et al. (2004, 2007, 2009). In addition to the taxonomic uncertainties reported above, the finding of central Mediterranean specimens clustering with Indo-Pacific specimens and of eastern Mediterranean specimens clustering with Atlantic specimens, suggests that one lineage (recently spreading in the central Mediterranean Sea) has to be considered alien, whilst another lineage (the eastern Mediterranean one) may be native to the area (Andreakis et al. 2004, 2007, 2009; Dijoux et al. 2014).
Presence in the Egadi Islands MPA: the first record of specimens belonging to this complex of species from the Egadi Islands MPA dates back to 2000 at Favignana (Barone et al. 2003a). From then on, its presence was regularly recorded at Favignana, both on the northern and the southern side, from sea level to 30 m depth (but mainly down to 20 m) on rock and sand, or as an epiphyte on Posidonia oceanica (Linnaeus) Delile, 1813 (R. D’Agostaro, unpublished data; P. Balistreri, unpublished data). In 2015, specimens belonging to this complex were also reported from Levanzo (P. Balistreri and A.M. Mannino, unpublished data). Unfortunately, no barcoding studies have been made on Aegadian material, although the molecular analysis of specimens from the nearby areas (Trapani and Pantelleria, Italy, and Mahdia, Tunisia) would suggest that specimens spreading in the Egadi Islands MPA belong to the Indo-Pacific clade. We therefore here consider this species as alien, pending further studies. Currently, the pathway of introduction (unaided spread or transport-stowaway) of local specimens cannot be attributed with certainty. Certainly, the Trapani coast, where it was first reported in 2000 (first Italian record; Barone et al. 2003b), might be considered a possible centre of secondary dispersal.
Bonnemaisonia hamifera Hariot, 1891
Status: ALIEN SPECIES
Remarks: believed to be native to Japan (Dixon and Irvine 1977). It reached the Mediterranean Sea by 1909, being first recorded at La Galite (Tunisia, Petersen 1918). Only “Trailiella-phase” (tetrasporophytic thallus) is known from the Mediterranean Sea. Transport-stowaway is considered the plausible pathway of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Levanzo (40 m depth) and Favignana (1 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Botryocladia madagascariensis G. Feldmann, 1945
Status: ALIEN SPECIES
Remarks: Madagascar is the type locality of this species. It was first reported from the Mediterranean Sea at Lampedusa Island and Castelluccio (Italy) in 1991 (Cormaci et al. 1992). Both unaided spread or transport-stowaway, through the Suez Canal, may be considered plausible pathways of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Favignana (0, 1 and 7 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Caulerpa cylindracea Sonder, 1845
(Fig. 2c)
Status: ALIEN SPECIES
Remarks: Until Belton et al. (2014), this species was often reported in the literature as Caulerpa racemosa var. cylindracea (Sonder) Verlaque, Huisman and Boudouresque. Native to Australia and New Caledonia (Belton et al. 2014), Caulerpa cylindracea Sonder, 1845 was first observed in the Mediterranean Sea in 1990 off the coast of Libya (Nizamuddin 1991).
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2003 at Favignana (Piazzi et al. 2005) and then in 2004 at Levanzo (ISPE 2007). The species was found on rock and sand in different habitats (e.g. P. oceanica meadows, vermetid reefs), both at sea level and between 15 and 30 m depth. Currently, C. cylindracea is widely distributed in the Egadi Islands. Unaided spread or transport-stowaway may both be plausible pathways of introduction for local specimens. Since it is a highly successful and fast-spreading species showing invasive behavior, in 2014 a public awareness project “Caulerpa cylindracea - Isole Egadi” was launched with the aim of creating a database on the dynamics of spreading and the invasiveness of C. cylindracea within the Egadi Islands MPA.
Caulerpa taxifolia (M. Vahl) C. Agardh, 1817 (invasive aquarium strain)
(Fig. 2d)
Status: ALIEN SPECIES
Remarks: originally described from the Virgin Islands (western Atlantic Ocean), Caulerpa taxifolia (M. Vahl) C. Agardh, 1817 was first recorded from the Mediterranean in 1984, where it was accidentally introduced by the Oceanographic Museum of Monaco (Meinesz and Hesse 1991; Jousson et al. 1998). Since then, the C. taxifolia invasive aquarium strain, genetically different from the ancestral Australian strain (Meusnier et al. 2004; Jongma et al. 2013), rapidly became widespread in the northwestern Mediterranean Sea (Meinesz et al. 2001).
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2004 at Favignana (Gianguzza et al. 2006). It was found from sea level to 22 m depth on sand, mostly in P. oceanica and Cymodocea nodosa (Ucria) Ascherson, 1870 meadows. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Ceramium strobiliforme G.W. Lawson & D.M. John, 1982
Status: ALIEN SPECIES
Remarks: Ghana is the type locality of this species. It was first reported from the Mediterranean Sea at Salina Island (Italy) in 1991 (Cormaci et al. 1992). Transport-stowaway is considered the plausible pathway of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Levanzo (0, 10 and 40 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Laurencia caduciramulosa Masuda & Kawaguchi, 1997
Status: ALIEN SPECIES
Remarks: Vietnam is the type locality of this species. It was first reported from the Mediterranean Sea at Lachea Island (Italy) in 1991 (Furnari et al. 2001). Transport-stowaway may be considered the plausible pathway of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Favignana and Marettimo (0 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Lophocladia lallemandii (Montagne) F. Schmitz, 1893
Status: ALIEN SPECIES
Remarks: The Red Sea is the type locality of this species. It was first reported from the Mediterranean Sea in Greece and Lybia in 1908 (Petersen 1918). Unaided spread through the Suez Canal is considered the plausible pathway of introduction in the Mediterranean Sea. This species, widespread throughout the tropics and subtropics (Boudouresque and Verlaque 2002), exhibits invasive behavior.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Favignana (7 m depth), Levanzo (1, 10 and 20 m depth) and Marettimo (25 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Neosiphonia harveyi (J.W. Bailey) M.S. Kim,
H.G. Choi, Guiry & G.W. Saunders, 2001
Status: ALIEN SPECIES
Remarks: Connecticut (USA) is the type locality of this species. It was first reported from the Mediterranean Sea in the Thau Lagoon (France) in 1958 (Lauret 1967 as Polysiphonia mottei Lauret). Escape from aquaculture facilities (according to CBD 2014) is considered the plausible pathway of introduction in the Mediterranean Sea.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Favignana (20 m depth) and Levanzo (10 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Womersleyella setacea (Hollenberg) R.E. Norris, 1992
Status: ALIEN SPECIES
Remarks: It is native to tropical areas with the Hawaiian Islands considered the type locality. It was first reported from the Mediterranean Sea in 1986 in Italy as Polysiphonia sp. (Benedetti-Cecchi and Cinelli 1989) and in France in 1987 as Polysiphonia setacea Hollenberg (Verlaque 1989). Transport-stowaway is suggested to be the plausible pathway of introduction in the Mediterranean Sea. This species is considered one of the most harmful invasive species (Boudouresque and Verlaque 2002).
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2001 at Favignana (1–7, 10, 20 and 30 m depth), Levanzo (0, 5, 10, 20, 30 and 40 m depth) and Marettimo (10 and 25 m depth) (Catra et al. 2006). There are no further records of this species in the area. Both unaided spread or transport-stowaway may be considered plausible pathways of introduction for local specimens.
Aplysia dactylomela Rang, 1828
(Fig. 2e)
Status: CRYPTOGENIC SPECIES
Remarks: originally considered a circumtropical species, recent molecular studies revealed that Mediterranean specimens belong to Aplysia dactylomela Rang, 1828 (originating from the Atlantic) rather than to its cryptic Indo-Pacific congeneric species Aplysia argus Rüppell & Leuckart, 1830 (see Valdés et al. 2013). Although the genetic composition of Mediterranean populations of A. dactylomela is consistent with a natural dispersal through the Strait of Gibraltar, the hypothesis of a human-mediated introduction in the Mediterranean from Atlantic populations cannot be discarded (Valdés et al. 2013). First recorded in the Mediterranean Sea from Lampedusa (Sicily Channel, Italy) (Trainito 2003), its Mediterranean introduction vector is not yet established with certainty (see discussions above), and therefore we cautiously considered this species as cryptogenic.
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA in 2013 at Favignana, likely dispersed naturally with veliger larvae carried by the current or by marine traffic (Mannino et al. 2014). Other records come from Favignana (Cala Moni), between 0 and 1.5 m on rock and sand, and from Marettimo (Scalo Vecchio), at 5 m depth on rocks. The presence of a few specimens may either be the result of a recent event, and new populations will soon be sighted in the whole Egadi Islands and on the western and southern coasts of Sicily (Mannino et al. 2014), or the result of the low phase of the population cycle (Carefoot 1987; Pennings 1991). The presence of A. dactylomela in the Egadi Islands MPA might be a consequence of unaided spread by dispersal of larvae, as already hypothesised by Valdés et al. (2013) to explain its introduction in the Mediterranean Sea.
Percnon gibbesi (H. Milne Edwards, 1853)
(Fig. 2f)
Status: CRYPTOGENIC SPECIES
Remarks: a native Atlantic species, first recorded in the Mediterranean Sea in 1999 at Linosa (Pelagian Islands, Sicily Strait) (Relini et al. 2000). There is a general agreement to include Percnon gibbesi (H. Milne Edwards, 1853) among Mediterranean aliens. However, due to the large planktonic duration of its larvae that leads to long-range dispersal (Paula and Hartnoll 1989; Katsanevakis et al. 2011), Abelló et al. (2003) suggest that this species entered the Mediterranean transported by the Atlantic current and its spread was through natural dispersal. Given wide uncertainties regarding possible vectors, and as there are no molecular studies carried out to date, we hereby cautiously considered this species as cryptogenic.
Presence in the Egadi Islands MPA: first found in the Egadi Islands MPA in August 2003, when several specimens were observed on the northern side of Marettimo (Scalo Maestro, Libano and Punta Due Frati), on a rocky bottom at 1.5 m depth (P. Balistreri, unpublished data). One of these, a male specimen (carapace: 17.5 mm width and 17.0 mm length) has been deposited in the Casa Museo “Matteo Sercia” of Favignana with the accession number CCGS0002. In July 2010, the species was also recorded from Favignana, at Pirreca (on the south-western side) at 1 m depth, at Scalo San Leonardo (harbour) at 1 m depth and in many other areas of the island (P. Balistreri, unpublished data) between 0 and 2 m depth. For P. gibbesi, the pathway of introduction (unaided spread or transport-stowaway) in the Egadi Islands MPA remains questionable.
Fistularia commersonii Rüppell, 1838
(Fig. 2g)
Status: ALIEN SPECIES
Remarks: native to and widely distributed in the Indo-Pacific, Fistularia commersonii Rüppell, 1838 is a highly successful Lessepsian migrant, first recorded in the Mediterranean Sea in 2000, along the coast of Israel at 35 m depth (Golani 2000), from where in few years it spread all over the Mediterranean Sea (Azzurro et al. 2013).
Presence in the Egadi Islands MPA: first reported from the Egadi Islands MPA at Marettimo in 2005 (Castriota et al. 2014). In November 2014, two specimens were caught, using a trammel net, at Favignana (Scoglio Corrente and Preveto Islet), on a rocky bottom at about 45 m depth (P. Balistreri, unpublished data). These specimens were fixed in alcohol and deposited in the Casa Museo “Matteo Sercia” (with the accession numbers CPOGS0001 and CPOGS0002, respectively). In November 2014, another specimen (about 90 cm long) was caught, using a trammel net, in the waters off Punta Mugnone (Marettimo), on a rocky bottom at about 20 m depth (P. Balistreri, unpublished data). For F. commersonii, unaided spread is considered the most probable pathway of introduction.
Kyphosus vaigiensis (Quoy & Gaimard, 1825)
(Fig. 2h)
Status: CRYPTOGENIC SPECIES
Remarks: a circumtropical species widely distributed both in the Atlantic and in the Indo-Pacific, often misidentified in the past as Kyphosus incisor (Cuvier, 1831), and recorded since 1998 from the Mediterranean Sea (Almuñécar, Granada, Spain) (see Mannino et al. 2015 for discussion and review). According to Zenetos et al. (2012), the records of this taxon should be considered as stemming from natural range expansion rather than human-mediated introduction. Mannino et al. (2015) recently discussed the status of Kyphosus vaigiensis (Quoy & Gaimard, 1825) in the Mediterranean, leaving open questions regarding a possible entry through the Suez Canal (including a transport-stowaway pathway) or the Strait of Gibraltar. Given the wide distribution reported in the literature, and being only recently recorded from the Mediterranean Sea, we here cautiously considered this species as cryptogenic.
Presence in the Egadi Islands MPA: a specimen molecularly identified as K. vaigiensis was first caught in September 2013 off Favignana, in shallow waters (approximately 3 m depth) on a hard bottom (Mannino et al. 2015). For K. vaigiensis, an unaided spread from neighbouring areas is a plausible pathway of introduction.
Stephanolepis diaspros Fraser-Brunner, 1940
(Fig. 2i)
Status: ALIEN SPECIES
Remarks: widely distributed in the Indo-Pacific, and first recorded in the Mediterranean Sea in the Levantine Basin in 1927 (Steinitz 1927). Stephanolepis diaspros Fraser-Brunner, 1940 is considered one of the earlier Lessepsian immigrants and is actually established in the whole eastern part of the basin (Golani et al. 2015) and well distributed in its central part (Lipej et al. 2014; Deidun et al. 2015; Golani et al. 2015).
Presence in the Egadi Islands MPA: in 2014, an adult male of this species (about 17 cm long) was caught using a trammel net in the waters off Punta Mugnone (Marettimo), on a rocky bottom at about 20 m depth (Balistreri and Parasporo in Tsiamis et al. 2015). For S. diaspros, an unaided spread from neighbouring areas may be a plausible pathway of introduction (see Deidun et al. 2015).
Conclusions
As already mentioned above, the overall approach of this article has been precautionary. Indeed, for species capable of active or passive propagule dispersal, it may be difficult to establish their status with certainty from faunal data only (e.g. if a species is an alien or simply a naturally spreading species). Recently, Marchini et al. (2015) stressed the need for standardised definitions and criteria in compiling inventories of marine alien species. Yet, the inclusion or not of a species among aliens is often purely a matter of semantics. Some of the species considered as cryptogenic may turn out to be recent natural entries in the Mediterranean Sea, but since they show invasive behavior, a careful monitoring of their spreading may be necessary independently from whether or not they are aliens.
Among the species listed here from the Egadi Islands MPA, macrophytes are the dominant group. The overall analysis of published and unpublished sightings (Table 2) clearly shows that Favignana is the island of the Egadi Islands MPA most affected by the introduction of alien and cryptogenic species, with species widely distributed all around the coastline. This is consistent with the central position of Favignana, both from a geographical and a transport-stowaway point of view; it is the island nearest to the Trapani coast and it is the one with more intense traffic of recreational, fishing or commercial boats, and with more tourists.
The identification of pathways of introduction of alien species at regional and local levels is a priority in order to manage the spread of species already introduced and to adopt preventive measures. The analysis of possible pathways of introduction in the Egadi Islands MPA showed that unaided spread is a plausible vector of arrival in the area for all the species analysed. However, a transport-stowaway (e.g. fishing, recreational boating, tourism)-mediated introduction cannot be totally rejected for several of the taxa listed, including all macrophytes, also considering the dynamics of spreading of these macrophytes after their entrance in the Mediterranean Sea.
Maritime traffic, visits by boats, ports and marinas may certainly lead to an increase of marine introductions, and can produce a constant spillover of new invaders into surrounding areas such as MPAs, contributing to their successful establishment (Otero et al. 2013). In agreement with the hypothesis suggested for other archipelagos (e.g. Evans et al. 2015; Schembri et al. 2015), we think that the regular and heavy transport-stowaway (recreational and/or commercial) potential between Sicily and the Egadi Islands MPA, and particularly Favignana, may have contributed to the arrival of sessile taxa often recorded in fouling communities. Whatever the true pathway (unaided spread or transport-stowaway), Sicily and/or the surrounding islands may represent an important centre of secondary dispersal for the Egadi Islands MPA.
All the species listed were recorded after the Egadi Islands MPA was established, with the first record dating back to 2000. However, this does not allow us to draw any conclusions about the effectiveness or ineffectiveness of the MPA in stopping local introductions. Indeed, this may be easily explained by the recent increase in research programs on marine reserves. Since areas located at the crossroads between the eastern and western sectors of the Mediterranean, like Sicily and the circum-Sicilian islands, are more vulnerable to marine biological invasions, regular monitoring programs, including public awareness campaigns, are strongly needed not only within MPAs but also in their surroundings in order to manage continuous spillover effects (see also Otero et al. 2013).
Moreover, in spite of their fundamental role in conservation of marine biodiversity, MPAs have been widely demonstrated to be ineffective in stopping local introductions, and therefore an invasive alien species (IAS) strategy integrated into the management plan may be highly desirable.
The creation of a permanent observatory involving all Sicilian MPAs, able to early detect new introductions and to follow the spread of species already present might be an effective tool in the management of present and future introductions of alien species in the MPAs and in neighboring areas.
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Acknowledgments
The authors thank Ernesto Azzurro, Luca Castriota, Stefano Melchioni, Gabriele Sercia, Vito Vaccaro and Bruno Zava for providing photos, information and records. They also thank Dr. Elisabetta Oddo for improving the English text. The study of the alien species from Italy was partially funded by the East and South European Network for Invasive Alien Species—a tool to support the management of alien species in Bulgaria (ESENIAS-TOOLS) (EEA funded: Contract No. Д-33-51/30.06.2015) (FC).
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Mannino, A.M., Parasporo, M., Crocetta, F. et al. An updated overview of the marine alien and cryptogenic species from the Egadi Islands Marine Protected Area (Italy). Mar Biodiv 47, 469–480 (2017). https://doi.org/10.1007/s12526-016-0496-z
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DOI: https://doi.org/10.1007/s12526-016-0496-z