Mediterranean Marine Science Review Article Indexed in WoS (Web of Science, ISI Thomson) The journal is available on line at http://www.medit-mar-sc.net Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution A. ZENETOS 1, S. GOFAS 2, M. VERLAQUE 3, M.E. INAR 4, J.E. GARCI’A RASO 5, C.N. BIANCHI 6, C. MORRI 6, E. AZZURRO 7, M. BILECENOGLU 8, C. FROGLIA 9, I. SIOKOU 10 , D. VIOLANTI 11 , A. SFRISO 12 , G. SAN MART N 13 , A. GIANGRANDE 14 , T. KATA AN 4, E. BALLESTEROS 15 , A. RAMOS-ESPLA ’16 , F. MASTROTOTARO 17 , O. OCA A 18 , A. ZINGONE 19 , M.C. GAMBI 19 and N. STREFTARIS 10 1 Institute of Marine Biological Resources, Hellenic Centre for Marine Research, P.O. Box 712, 19013 Anavissos, Hellas 2 Departamento de Biologia Animal, Facultad de Ciencias, Universidad de Ma ’laga, E-29071 Ma ’laga, Spain 3 UMR 6540, DIMAR, COM, CNRS, Université de la Méditerranée, France 4 Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100 Bornova, Izmir, Turkey 5 Departamento de Biologia Animal, Facultad de Ciencias, Universidad de Ma ’laga, E-29071 Ma ’laga, Spain 6 DipTeRis (Dipartimento per lo studio del Territorio e della sue Risorse), University of Genoa, Corso Europa 26, 16132 Genova, Italy 7 Institut de Ciències del Mar (CSIC) Passeig Mar tim de la Barceloneta, 37-49, E-08003 Barcelona, Spain 8 Adnan Menderes University, Faculty of Arts & Sciences, Department of Biology, 09010 Aydin, Turkey 9 c\o CNR-ISMAR, Sede Ancona, Largo Fiera della Pesca, 60125 Ancona, Italy 10 Institute of Oceanography, Hellenic Centre for Marine Research, P.O. Box 712, 19013 Anavissos, Hellas 11 Dipartimento di Scienze della Terra, University of Turin, via Valperga Caluso 35, 10125 Torino, Italy 12 Department of Environmental Sciences, University of Venice, Calle Larga 2137, 30123 Venice, Italy 13 Departamento de Biolog a (Zoolog a), Facultad de Ciencias, Universidad Auto ’noma de Madrid, calle Darwin, 2, 28049 Madrid, Spain 14 Department of Biological and Environmental Sciences and Technologies, University of Lecce, Complesso Ecotekne, Via Prov. le Lecce-Monteroni, 73100 Lecce, Italy 15 Centre d’Estudis Avanç ats de Blanes (CSIC), Acc. Cala, Sant Francesc 14, 17300 Blanes, Girona, Spain 16 Centro de Investigacio ’n Marina de Santa Pola (CIMAR), Universidad de Alicante, 03130 Santa Pola, Alicante, Spain 17 Department of Biology, University of Bari, Via Orabona 4, 70125 Bari, Italy 18 Departamento Oceanograf a Biolo ’gica y Biodiversidad, Fundacio ’n Museo del Mar Muelle Can~onero Dato S/N 51001, Ceuta, Spain 19 Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy Corresponding author: [email protected] Medit. Mar. Sci., 11/2, 2010, 381-493 381 http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 06/03/2019 12:32:23 | Abstract The state-of-art on alien species in the Mediterranean Sea is presented, making distinctions among the four subregions defined in the EU Marine Strategy Framework Directive: (i) the Western Mediterranean Sea (WMED); (ii) the Central Mediterranean Sea (CMED); (iii) the Adriatic Sea (ADRIA); and (iv) the Eastern Mediterranean Sea (EMED). The updated checklist (December 2010) of marine alien species within each subregion, along with their acclimatization status and ori- gin, is provided. A total of 955 alien species is known in the Mediterranean, the vast majority of them having being introduced in the EMED (718), less in the WMED (328) and CMED (267) and least in the Adriatic (171). Of these, 535 species (56%) are established in at least one area. Despite the collective effort of experts who attempted in this work, the number of introduced species remains probably underestimated. Excluding microalgae, for which knowledge is still insuffi- cient, aliens have increased the total species richness of the Mediterranean Sea by 5.9%. This figure should not be directly read as an indication of higher biodiversity, as spreading of so many aliens within the basin is possibly causing biotic homogenization. Thermophilic species, i.e. Indo-Pacific, Indian Ocean, Red Sea, Tropical Atlantic, Tropical Pacific, and circum(sub)tropical, account for 88.4% of the introduced species in the EMED, 72.8% in the CMED, 59.3% in the WMED and 56.1% in the Adriatic. Cold water species, i.e. circumboreal, N Atlantic, and N Pacific, make up a small percentage of the introduced species, ranging between 4.2% and 21.6% and being more numerous in the Adriatic and less so in the EMED. Species that are classified as invasive or potentially invasive are 134 in the whole of the Mediter- ranean: 108 are present in the EMED, 75 in the CMED, 53 in the Adriatic and 64 in the WMED. The WMED hosts most invasive macrophytes, whereas the EMED has the lion’s share in poly- chaetes, crustaceans, molluscs and fish. Keywords: Biological invasions; Marine aliens; Biogeography; Biodiversity; Mediterranean Sea. Introduction In 1978, there were 128 proven Lessepsian immigrants and 76 doubtful The Mediterranean Sea is one of the cases (POR, 1978). Since the first review seas of the world most affected by biolog- of alien species in the Mediterranean ical invasions in terms of how long the (ZIBROWIUS, 1992), there have been invaders hav e been present (OCCHI- many papers and reviews dealing with this PINTI-AMBROGI, 2000; STREFTARIS subject. More recently, CIESM has pub- et al., 2005), in number of alien species lished four Atlases of Exotic Species in detected (COSTELLO et al., 2010) and in the Mediterranean (GALIL et al., 2002; the unprecedented rate of introduction GOLANI et al., 2002; ZENETOS et al., (ZENETOS, 2009; 2010). Triggered by 2004; VERLAQUE et al., in press). The warming waters and a newly improved most recent lists show 116 species of fish- route through the Suez Canal, es, 70 species of decapod and stomatopod tropical/subtropical marine species, some crustaceans, 137 species of molluscs and very invasive, have progressively moved 110 species of macrophytes. This into the Mediterranean, disrupting increased number of records, particularly ecosystem stability of the basin. over the past few years, has been partly 382 Medit. Mar. Sci., 11/2, 2010, 381-493 http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 06/03/2019 12:32:23 | attributed to intensification of research emergence of the new generation of EU effort in this topic. ZENETOS & political actions covering major maritime POLYCHRONIDIS (2010), based on strategic objectives, such as the Marine data gathered, analysed for and adopted Strategy Framework Directive (MSFD) in the European Environment Agency (2008/56/EC), the European Strategy for (EEA) and UNEP MAP RAC/SPA Marine and Maritime Research (COM reports, estimated that nearly 1000 (2008) 534) encompassing the Marine species entered the Mediterranean dur- Spatial Planning and the Ecosystem ing the past century. Approach (ECAP) within the Barcelona A recent synthesis on Mediterranean Convention by UNEP/MAP 1, as well as marine biodiversity (COLL et al., 2010) many initiatives of the UNEP RAC/SPA. described the Mediterranean Sea as a Alien species regulations are of major biodiversity hot spot hosting approxi- importance in those policies. In the cur- mately 17,000 marine species, of which rent MSFD the descriptor: "Non-indige- more than 600 (3.3%) are alien. These nous species introduced by human activi- most recent detailed biodiversity esti- ties are at levels that do not adversely mates for alien species show a discrepan- alter the ecosystems" is actually one of the cy from the figures provided by eleven qualitative descriptors for deter- ZENETOS et al. (2005; 2008). However, mining Good Environmental Status as COLL et al. (2010) have pointed out, (GES). It is also closely related to six the true numbers of alien species are cer- other GES descriptors because of the tainly biased downwards. The data are great variety of impacts that Invasive presumably accurate for large and con- Alien Species (IAS) may exert on native spicuous species that are easily distin- biodiversity, ecosystem functioning, and guished from the native biota and for seabed habitats as well as commercial species that occur along a frequently sam- marine resources (OLENIN et al., 2010). pled (or fished) coast and for which taxo- This territorial and institutional sce- nomic expertise is readily available, but nario raises the need for a multi-level are entirely absent for many of the small governance system with a quite complex members of invertebrates. This under- coordination system in which non-EU representation is common in many works Member States can also participate. This and efforts have been made to include is particularly important in the Mediter- less studied groups in recent reviews (see ranean, where the southern and eastern ZENETOS et al., 2008). coast belong to non-EU Member States An up-to-date inventory of the alien or countries with accession status (e.g. species in the Mediterranean, apart from Turkey and Israel). Furthermore, the its scientific merits, can fulfil the needs of Barcelona Convention of the UNEP/MAP the regulatory requirements and environ- supports the introduction of MSFD mental management options. This is of (2009) concepts that can be useful particular importance since the current throughout the basin despite the handi- 1 The Barcelona Convention of the UNEP/MAP supports the introduction of MSFD in the Mediterranean. To that end, they are following the ecosystem approach (including the concept of policy steps), which is the priority of the recently adopted 5-year programme. Presently they are working on assessing the state of the environment, includ- ing economic and social aspects, in the four subregions. Medit. Mar. Sci., 11/2, 2010, 381-493 383 http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 06/03/2019 12:32:23 | cap that only seven of 21 Mediterranean studied along the four subregions as countries are Member States of adopted and described under the MSFD.