East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea

Accepted Manuscript East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea Bella S. Galil, Agnese Marchini, Anna Occhipinti-Ambrogi PII:

S0272-7714(15)30176-1

DOI:

10.1016/j.ecss.2015.12.021

Reference:

YECSS 4993

To appear in:

Estuarine, Coastal and Shelf Science

Received Date: 16 March 2015 Revised Date:

1 December 2015

Accepted Date: 22 December 2015

Please cite this article as: Galil, B.S., Marchini, A., Occhipinti-Ambrogi, A., East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea, Estuarine, Coastal and Shelf Science (2016), doi: 10.1016/j.ecss.2015.12.021. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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East is east and West is west? * Management of marine bioinvasions in the Mediterranean Sea

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*Kipling R. (1889) The Ballad of East and West.

Bella S. Galil1, Agnese Marchini2, Anna Occhipinti-Ambrogi2 1

National Institute of Oceanography, Israel Oceanographic and Limnological Research, Tel Shikmona, P.O. Box

Department of Earth and Environmental Sciences, University of Pavia, Via S. Epifanio, 14, I-27100 Pavia, Italy

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8030, Haifa 31080, Israel

Abstract

At 726 the number of recorded multicellular non indigenous species (NIS) in the Mediterranean Sea is far higher than in other European Seas. Of these, 614 have established populations in the

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sea. 384 are considered Erythraean NIS, the balance are mostly ship and culture-introductions. In order to effectively implement EU Regulation on the prevention and management of the introduction and spread of invasive NIS and the Marine Strategy Framework Directive in the Mediterranean Sea it is crucial that this priority pathway is appropriately managed. Three

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potential impediments – incomplete and inaccurate data; unknown impacts; policy mismatch – hinder implementation. Current geographical, taxonomical and impact data gaps will be reduced only by instituting harmonized standards and methodologies for monitoring NIS populations in

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all countries bordering the Mediterranean Sea, prioritizing bridgehead sites and dispersal hubs. The option of implementing European environmental policies concerning marine NIS in member states alone may seem expedient, but piecemeal protection is futile. Since only 9 of the 23 states bordering the Mediterranean are EU member states, the crucial element for an effective strategy for slowing the influx of NIS is policy coordination with the Regional Sea Convention (Barcelona Convention) to ensure consistency in legal rules, standards and institutional structures to address all major vectors/pathways. 1

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Highlights: 384 of the 614 NIS established in the Mediterranean were introduced via Suez Canal

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Erythraean NIS expanded westwards and northward in the past two decades

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To comply with regulations priority pathways should be appropriately managed

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Regulation enforcement depends on policy coordination with non EU Member States

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data gaps reduced by standardizing methodologies in all Mediterranean countries

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precautionary principle

1. INTRODUCTION

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Keywords: Mediterranean Sea, non indigenous species, priority pathway, Suez Canal,

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The spread of NIS is one aspect of global change in the marine environment (Dukes & Mooney, 1999; Occhipinti-Ambrogi, 2007; Austen et al., this issue). The environmental implications of marine NIS are of deep concern to scientists, legislators and management (Williams & Grosholz, 2008; Hewitt et al., 2009; Ojaveer et al., 2014).

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The EU Regulation on the prevention and management of the introduction and spread of invasive alien species (IAS Regulation) (EC, 2014) and the Marine Strategy Framework Directive (MSFD), where NIS

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constitute part of the evaluation of ‘Good Environmental Status’ (GES) (EC, 2008; EC, 2010), acknowledge the critical role of vectors in biological invasions and consider it crucial to manage the pathways. The general provisions ask Member States to “carry out a comprehensive analysis of the pathways of unintentional introduction and spread of invasive alien species in their territory and identify the pathways which require priority action (priority pathways), because of the volume of species or of the damage caused by the species entering the Union through them.” (EC, 2014, Art.13.1).

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The Mediterranean Sea has a long history of bioinvasions: of the 22 NIS recorded in the Mediterranean before 1900, 11 are considered to have entered the sea through the Suez Canal, heralding the Erythraean invasion; 8 were likely ship-transported and 2 early culture introductions. Thirteen of the 14 NIS recorded for the first time in the Mediterranean in the first

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decade of the 20th century entered through the Suez Canal (Galil, 2012). The number of records of species introduced into the Mediterranean is by far the highest compared with other European Seas: nearly triple the number of records known from the Western European Margin stretching

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from Norway to Portugal (Galil et al., 2014).

In this paper we identify and discuss issues relating to the assessment of spatial and temporal

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patterns of NIS in the Mediterranean Sea. While recognizing the limitations of the existing data, it serves to manifest trends in species numbers, temporal occurrence and spatial distribution in relation to the main vectors, as required by the MSFD and IAS regulation. Based on these data, realistic and practicable priority actions are proposed to ameliorate potential impediments that

2. METHODS

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hinder their implementation.

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We follow the definition set out in Annex 1 of MSFD, and refer to NIS as species introduced by human activities (EC, 2008). The term invasive is associated with “adverse effects…. on biodiversity and related ecosystem services, and on human health and safety as well as… their

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social and economic impact” (EC, 2014, Art. 6). Since scientifically validated data concerning the adverse effects of marine NIS is sparse (Ojaveer et al., 2015) we use here the term widespread as surrogate, referring to one component of invasiveness, i.e. the spatial spread of NIS. We consider here widespread species recorded in 10 or more Mediterranean countries (Galil et al., 2014). Species which populations undergo climate-shifted spread are not considered as NIS (EC, 2014, Art. 2.2a). We limit the database to multicellular organisms as, with a few exceptions (Schimdt et al., 2015), the identity and origin of many unicellular taxa is in doubt and subject to ongoing revisions (Gomez, 2008; Zenetos et al., 2012; Meriç et al., in press). We 3

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distinguish ‘established’ NIS (species recorded several times, or in several localities, or abundant), from ‘single records’ (one or few specimens recorded once in a single location) and from NIS whose populations are known to be extinct. Single records NIS whose populations are known to be extinct were removed from our analysis, as well as species recorded once in a single

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location, as they are considered either ephemeral introduction (if the record is decades old), or possibly not yet established as an enduring self propagating population (if the record is recent,

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i.e. within the past decade).

Previous studies (Galil et al., 2014) were expanded to capture recent records (to 2015), as well as previously overlooked records. Published inventories of NIS in the Mediterranean were cross-

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compared and judiciously examined, authors were contacted for supplementary information when needed, and taxonomists were consulted in order to maintain a high level of scholarship and consistency (see acknowledgments). Following Marchini et al. (in press), dubious records were excluded pending confirmation. The latter include records affected by uncertainty regarding:

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(i) species identity, i.e. taxa identified to genus or higher level, species with unresolved taxonomic status (species complex or morphologically similar taxa), records lacking proper scientific documentation (species only mentioned in faunal inventories and lists, conference abstracts without proper descriptions);

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(ii) non indigenous status, i.e. cryptogenic species sensu Carlton (1996), species which are naturally expanding their range (see above); native Mediterranean species transferred to new

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Mediterranean areas by human intervention; (iii) occurrence in the Mediterranean Sea, i.e. species recorded in water bodies adjacent to the sea but lacking direct connections with the sea, non-living records (i.e., loose valves, empty shells), species recorded only from vectors (e.g. vessel ballast tanks, hulls, gas or oil platforms, fisheries, culture and seafood equipment).

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The data were collected and organized to be included in AquaNIS, a pan-European aquatic nonindigenous and cryptogenic species information system (www.corpi.ku.lt/databases/aquanis, version 2.3), though cryptogenic species were excluded (see above).

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For most Mediterranean countries (Fig. 1) a list of NIS was assembled, comprising the date and location of first record, subsequent records where available, pathway/vector, region of origin, habitat, and status of population. The date of first record is the year of collection, or when unknown, the date of publication. For some earlier records, which first introduction event is

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uncertain, a time range was indicated instead. For some NIS which had been originally described from the Mediterranean (e.g. Littorina saxatils type material collected in the Lagoon of Venice, Italy) the year of description was used, though its introduction may have occurred centuries

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earlier. We list the pathway/vector where it is known from direct evidence (e.g. documented intentional introductions), or associated with them, e.g. found in, or adjacent to, ports (vessels), shellfish-farms (culture). NIS recorded in the Levant, which occurs in the western Indian Ocean, Red Sea or Suez Canal is considered to have entered through the Suez Canal (Erythraean). When more than a single vector may be implicated, they are cited in order of likelihood, e.g. Suez Canal, Vessels, Culture, Vessels. The status of the population was categorized in increasing order

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from single record (see above), rare (few individuals recorded), local (common in a restricted range), common (commonly recorded in a particular habitat), abundant (large number of individuals commonly recorded), unknown (no information was available to us on the population status). Regions of origin, and status of population, were derived from the literature and from

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communications with regional experts.

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Data for countries with 50 or more established NIS (see above) were analyzed for number of species recorded per decade, cumulative number of species identified by vector, taxa, region of origin, percentage of first Mediterranean records per total NIS, species recorded in 10 or more of the Mediterranean countries. The data for each of Italy’s regions (Adriatic Sea, Ionian Sea and Sicily Straits, Tyrrhenian and Ligurian Seas) was analyzed separately, being at the crossroads between eastern and western Mediterranean (Occhipinti-Ambrogi et al., 2011).

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We used the Bray-Curtis similarity index (Bray & Curtis, 1957), based on the presence/absence of established NIS, to identify patterns of regional distribution. A basic agglomerative hierarchical cluster algorithm was run using the group average approach, which defines cluster proximity as the average pairwise proximity of all pairs of points from different clusters. A

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SIMPER test allowed identification of NIS most responsible of similarity within groups. The multivariate analysis was carried out using the computer program PRIMER v. 6 (Primer-E Ltd.,

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Plymouth, UK).

3. RESULTS

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3.1 Number of NIS

A total of 726 multicellular NIS were recorded, of which 112 are single or extinct records. For example, Notopus dorsipes (Linnaeus, 1758) or Panulirus ornatus (Fabricius, 1798), never observed since their original records in 1962 and 1988 respectively, or Saccostrea glomerata (Gould, 1850), experimentally introduced to the Venice Lagoon in 1984 but unable to survive,

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have been omitted from the analysis. The number of established NIS, after excluding extinct and single records, is 614 (listed in the Supplementary material). The number of NIS differs among the Mediterranean countries, and is substantially greater in the east than in the west Mediterranean. Of the 614 established NIS, 324, 295, 190 and 175 species were recorded off

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Israel, Turkey, Lebanon and Egypt respectively, as compared with 105 and 69 from the Mediterranean coasts of France and Spain (Fig. 2). The number of established NIS recorded in

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the different coasts of Italy is given in Fig. 3.

3.2 Temporal trend of introductions

The total number of NIS recorded in the Mediterranean more than doubled (223%) between 1970 and 2015 (Fig. 4a), with the greatest increase recorded in the 1990s and the 2000s (Fig. 4b).

3.3 Differences among Mediterranean countries 6

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Patterns of regional distributions were revealed, based on the shared and unique established NIS records. Analysis of the 1738 introduction records in the 11 countries with more than 50 records of established NIS, displays a Levantine cluster (Israel, Turkey, Lebanon, Egypt, Syria, Cyprus,

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Greece; 48% similarity), allied (at 31% similarity) with Tunisia. France and Spain form a cluster (at 42% similarity), whereas Italy is distinct (less than 10%) (Fig. 5).

Data for 8 of the 11 countries with 50 or more established NIS (Egypt, Israel, Turkey, Greece,

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Tunisia, Italy, France and Spain) were analyzed for vectors of introduction, native origin, and composition of taxa (Fig. 6a-c). Distinct patterns in NIS numbers are evident for eastern and western countries, yet all show an increase in records. The Levantine countries (Egypt, Israel,

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Turkey, Greece), and to lesser degree Tunisia, saw an increase in the number of introductions through the Suez Canal (as well as Cyprus, Lebanon and Syria, not shown); in Italy and Spain the majority of recent records stems from shipping, whereas in France shipping and mariculture introduced nearly equal number of species (Fig. 6a). Most introductions in the Levant and Tunisia originated in the tropical/subtropical Indo-Pacific Ocean; Italy, France and Spain likewise saw a rise in thermophilic NIS. Fish, mollusks and crustaceans are the major taxa

and Spain.

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introduced to the Levant, whereas macroalgae account for the highest number in Italy, France

The comparative analysis among graphs in Fig. 6a-c shows that vectors determine the

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geographical origin and the introduced taxa: in countries where the Suez Canal is the main vector (Egypt, Israel, Turkey), most NIS are of tropical/subtropical Indo-Pacific origin and comprise

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molluscs, fish and crustaceans, i.e. taxa actively spreading as adults or more passively transported as larvae. In countries where vessels and aquaculture are the prevailing vectors (Italy, France, Spain), the taxonomic composition and native ranges of NIS are more diverse and depend on shipping routes and mariculture trades. In France, where aquaculture is the main vector, a large number of species are of subtropical/temperate Pacific origin, and are mainly represented by macroalgae, often associated with imported shellfish. Spain, where shipping mainly determines introductions, features a large array of taxa from many world regions. The Italian data (Fig. 3) shows that the main vectors in the Adriatic Sea were shipping and culture, 7

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the latter greatly increased in the 1990s; elsewhere, the major vector is shipping. A slight increase in the number of Erythraean introductions since the millennium is noted in the Ionian Sea and Sicily Straits as well as the Tyrrhenian and Ligurian Seas.

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3.4 First records in the Mediterranean

Israel has by far the highest number (200) and the highest percentage (62%) of earliest records in the Mediterranean Sea of established NIS (Table 1, Fig. 7). Of this number, 146 were

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subsequently recorded in other Mediterranean countries. Italy and France too have high percentage (about 53%) of first records and serve as beachheads and dispersal hubs for the

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secondary spread of shipping and culture-introduced species.

3.5 Temporal pattern of widespread species

Of the 614 established NIS, 138 are recorded in 5 or more countries, and 26 are recorded in 10 or more countries (Table 2). Of these, 15 species are considered introductions through the Suez Canal, whereas shipping and culture introduced 8 and 2 species, respectively. The great majority

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of the widespread species have been established in the sea for many decades - the average time elapsed since the first record for the widespread species is 87 ± 40 years. Only four widespread species - Caulerpa cylindracea, Fistularia commersonii, Lagocephalus sceleratus and Percnon

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gibbesii - were recorded for the first time in the Mediterranean after 1970.

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4. DISCUSSION

The number of recorded introductions into Mediterranean Sea is far higher than in other European Seas (Galil et al., 2014). The total number of multicellular NIS (updated to 2015) having entered the Mediterranean Sea currently stands at 726. Of these species, 450 are considered Erythraean NIS. This influx has profoundly marked the composition of the biota of the southeastern Mediterranean Sea (Steinitz, 1970; Por, 1978; Galil, 2007a, 2009; Galil et al., 2014). 8

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The implementation of the IAS Regulation and the MSFD requires EU Member States bordering the Mediterranean Sea to draft a program of measures to achieve GES. More specifically, the IAS Regulation (EC, 2014, Art. 13) mandates “Member States shall, within 18 months of the

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adoption of the Union list carry out a comprehensive analysis of the pathways of unintentional introduction and spread of invasive alien species of Union concern at least in their territory, as well as in their marine waters … Within three years of the adoption of the Union list, each Member State shall establish and implement one single action plan or a set of action plans to

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address the priority pathways it has identified ... Action plans shall include timetables for action and shall describe the measures to be adopted and, as appropriate, voluntary actions and codes of

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good practice, to address the priority pathways and to prevent the unintentional introduction and spread of invasive alien species into or within the Union”. At the same time the Commission Decision on criteria and methodological standards on GES of marine waters (EC, 2010) calls for “Trends in abundance, temporal occurrence and spatial distribution in the wild of non-indigenous species, particularly invasive non-indigenous species, notably in risk areas, in relation to the

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main vectors and pathways of spreading of such species”.

Three principial impediments (incomplete and inaccurate data; unknown impacts; policy mismatch) have been identified that may constrain effective implementation of the IAS Regulation and the MSFD.

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4.1 Incomplete, inaccurate, uncertain data

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Historical and geographical data gaps, in addition to taxonomical identification issues, mean that for the greater number of NIS the date of collection may be years (even centuries in some cases) behind the actual date of introduction, and identification and publication may lag decades behind collection (Galil, 2007b; Bariche et al., 2014; Harmelin, 2014; Marchini et al., 2014). Marine NIS, particularly those belonging to smaller sized taxa, remain largely unrecognized and undetected. Targeted efforts to survey the presence and abundance of NIS have been spatially and temporally limited, and many of these studies are all too recent. For these reasons the numbers of records are likely to be grossly underestimated. Moreover, early human-mediated 9

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introductions into the Mediterranean Sea prejudice our understanding of invasion patterns and processes (Galil & Gevili, 2014). The data are presumably most accurate for large and conspicuous species, but increasingly used molecular tools have revealed cryptic species and erroneous identifications, as well as serving to identify their origin and source (Comtet et al.,

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2015). The magnitude of the gap is difficult to assess and differs among taxa, habitats and geographical regions (e.g., Tsiamis et al., 2010; Gravili et al., 2013). Research efforts doubtlessly play an important part: 324 established NIS have been reported from Israel as against 175 from Egypt; in Libya and Syria as well much lower numbers of NIS were recorded compared with

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their neighboring countries. Uncertainty also shrouds our assessment of pathway/vector. With the exception of documented intentional introductions (i.e. culture and stocking activities), the

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attribution of a vector (or multiple vectors in some cases) is speculative and direct evidence is scarce (Ruiz et al., 2000). Advances in molecular genetics help reconstruct introduction history, yet we are still far from a comprehensive molecular assessment of marine bioinvasions (Darling, 2015). We suggest that uncertainty concerning pathway/vector needs to be taken into account by management (Lee et al., 2010; Williams et al., 2013) and should not be excluded from analyses (Katsanevakis et al., 2014b).

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The diverse criteria adopted for compiling inventories of NIS induce dissimilar quantifications of xenodiversity. For example, two inventories of Italian marine NIS (European Alien Species Information Network on-line database and Italian Society of Marine Biology, GSA-SIBM, 2015) differ in over 100 records (Marchini et al., in press). While we excluded Oenone cf. fulgida for

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uncertain identity (Çinar, 2005), it was listed elsewhere (Katsanevakis et al., 2009, 2015; Zenetos et al., 2010); Acanthophora nayadiformis was omitted as a possible Tethyan relict

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(Cormaci et al., 2004), but listed elsewhere (Galil, 2009; Bazairi et al., 2013); we considered the west African Cephalopholis taeniops, recorded along the southern rim of the Mediterranean (Ben Abdallah et al., 2007; Salameh et al., 2009), as range expansion by a thermophilic species, yet it was listed as NIS elsewhere (Zenetos et al., 2010; Katsanevakis et al., 2011). Agreed-upon uniform criteria for the development of inventories of NIS based on solid and transparent scientific criteria are urgently required (Gatto et al., 2013; Ojaveer et al., 2014; Marchini et al., in press).

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Clarifying the identity, geographic origin and the pathways of introduction are of major importance for management of bioinvasions. Only when these are established, can specific and appropriate measures be devised and implemented. Molecular tools are widely relied upon to provide accurate data concerning these issues, and the veracity and accuracy of scientific articles

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are generally taken for granted, but questionable, and sometimes erroneous publications occur, though for the present their use is still limited to a small number of cases. It is necessary to expunge inaccurate, unsubstantiated or misleading statements before they slip into the scientific mainstream and the ubiquitous citation systems (Galil, 2012, 2015). The EEA, IAS Regulation

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and the MSFD rely on region-wide databases to identify and prioritize management decisions. With much at stake for scientists, regulators, and management, it is important that terminology

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and recording methods should be standardized.

Priority Actions: A. Reduce current geographical and taxonomical data gaps by instituting harmonized standards and methodologies for monitoring NIS populations in all countries bordering the Mediterranean Sea, prioritizing bridgehead sites and dispersal hubs. B. Ensure the accuracy, veracity and quality of data entries into national/regional datasets, and harmonize

4.2 Unknown impacts

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criteria and terminology.

According to the IAS regulation (EC, 2014), “a significant subset of alien species can … have a

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serious adverse impact on biodiversity and related ecosystem services, as well as have other social and economic impact, which should be prevented”. However, delineation of threat or

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impact levels is lacking for most marine NIS. Bioinvasion impacts have been poorly quantitatively or experimentally studied (Kumschick et al., 2015). This shortfall is even more glaring in marine bioinvasion impact assessments: Katsanevakis et al. (2014b), who sorted records of impacts of NIS in European seas according to their evidence (manipulative experiments, direct observations, natural experiments, modeling, non-experimental based correlations, expert judgement), concluded that evidence for most of the reported ecosystem impacts is weak, based on expert judgement or dubious correlations, only 13% resulted from manipulative or natural experiments. Similarly, impacts for the vast majority of Mediterranean 11

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NIS remain unknown, and the few cases studied are of insufficient temporal and spatial scales. In all cases, the cumulative and/or synergistic connections with other stressors affecting the marine environment are largely unknown. Entrapped in a ‘Catch 22’ situation (after J. Heller’s novel, a requirement that cannot be met until an unobtainable prerequisite requirement is met), the

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number of marine NIS with sufficient data to satisfy the criteria for ‘significant negative impact’ is meagre, because understanding of marine ecosystems functions is constrained due to lack of appropriately designed studies. Unless impacts are conspicuous, induce direct economic cost, or

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impinge on human welfare, they fail to arouse public awareness, funding, and scientific analysis. Ojaveer et al. (2015) state that the paucity of data impedes the understanding of invasion ecology and prioritizing conservation and research aims for marine ecosystems. It is imperative that until

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these gaps are filled, a precautionary approach prevails that would treat data deficient bioinvasions as representing an ‘unknown’ and, therefore, should be considered at a high level of risk. While waiting for the knowledge base to be acquired, we recommend using the ‘spatial extent’ concept of widespread species (Galil et al., 2014) as surrogate for potential disturbance of native communities.

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Priority Action: Focus research efforts on identification and quantitative assessment of the actual impacts of NIS in the Mediterranean. Until scientifically-validated results are available, the application of precautionary principle must remain in force, with management focussing on prevention of new incursions through management of invasion vectors and pathways, and where

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practicable, on beachhead sites to minimize secondary spread. 4.3 Policy mismatch

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The MSFD is a visionary science-driven initiative that aims to implement a holistic, ecosystembased policy. Among its many unique features is the bold acknowledgement that NIS represent one of the main threats to marine biodiversity and related ecosystem services, and placing them among the 11 qualitative descriptors for determining GES. Yet, of the 23 bordering states only 9 are EU Member States (UK (Gibraltar), Spain, France, Italy, Slovenia, Croatia, Malta, Greece, Cyprus) which poses a seemingly insurmountable challenge. Though States are responsible for ensuring that activities within their jurisdiction do not damage the environment of other States, 12

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for the IAS Regulation concerning marine NIS to be effective in the Mediterranean, implementation depends on policy coordination with the Regional Sea Convention (Barcelona Convention). However, the gap among member and non member states could not have been more apparent than during the Meeting of the Focal Points of the Mediterranean Action Plan

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(UNEP/MAP, 2013), that discussed adoption of Draft decision on the Ecosystems Approach including definitions of Good Environmental Status (GES) and targets, where inclusion of “invasive non-indigenous species introductions” was made conditional on “Excluding

introduction through the Suez Canal”. It may seem an expedient ‘compromise’ to the ‘focal

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points’, but this bureaucratic act of ‘denialism’ does not change the reality that the introductions through the Suez Canal contribute the largest number of NIS in the Mediterranean, affecting

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fisheries, tourism and human health.

The option of implementing the MSFD in Member States alone, where the main vectors are shipping and culture, is doubtlessly tempting, as regulations concerning ballast water and sediments and transfer of cultured biota are in effect, or shortly to be. But this is a short term solution at best. The most spatially extensive species spread after a long residency in the sea, so

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we may well expect the thermophilic Erythraean species which have been first recorded in the 1970s and 1980s or earlier to expand their range and spread westwards and northwards – the so called invasion debt. As the sea is warming the process may be accelerating (e.g., shoals of Portunus segnis in the Gulf of Gabes, Tunisia, J. Ben Souissi, pers. com. Oct. 2015). The

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enlargement of the Suez Canal increases the number of Erythraean propagules swept through. The individual and cumulative impacts of these species will affect the conservation status of

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native species and critical habitats, as well as the structure and function of ecosystems and the availability of natural resources, and may add to the number of Suez Canal-introduced species that are noxious, poisonous, or venomous and pose threats to human health (Galil et al., 2015). In the 1970s it was believed that the populations of the canal-introduced species will remain confined to the southeast Levantine Basin. We can no longer affect willful blindness – many of the Suez Canal-introduced species have spread throughout the eastern Mediterranean, and some, much farther: the lethally poisonous pufferfish Lagocephalus sceleratus has been recorded in 2014 both in Sevastopol, in the northeast of the Black Sea and in Spain (Izquierdo-Muñoz & 13

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Izquierdo-Gomez, 2014; Boltachev et al., 2014), the venomous jellyfish Rhopilema nomadica was recently recorded off Pantelleria, in the Strait of Sicily (S. Piraino, pers. com. Oct. 2015).

Priority actions: A. Undertake coordination and integration of policies through the Barcelona

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Convention to ensure consistency in legal rules, standards and institutional structures regarding MSFD Descriptor 2 (“Non- indigenous species introduced by human activities are at levels that do not adversely alter the ecosystem”) of all parties, Member States as well as non-EU Member States. B. Undertake a transparent and scientifically sound ‘Environmental Impact Assessment’

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(EIA) of transboundary impacts associated with Erythraean NIS.

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NEVER THE TWAIN SHALL MEET?

The historical track of records, critically revised and analysed, indicates that the global trend of increasing numbers of NIS is magnified in the Mediterranean Sea. In its western basin species have been introduced mainly through mariculture and shipping activities, whereas the Suez Canal has served as a conduit for thermophilic species from the Indian Ocean. However, in the past two decades the latter have been inexorably expanding westwards – 35 of the 48 established

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Erythraean species in Tunisia have been recorded since 1995 – modifying the historical differences in biological characteristics of the two Mediterranean regions and with implications for ecosystem services, human health and economic impact.

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In the framework of the EU efforts to limit the threat of IAS, the large number of NIS in the Mediterranean Sea warrants special attention. The influx of Erythraean NIS is no longer limited to the SE Levant, its effects are already felt in the central Mediterranean, and with ongoing

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warming they are likely to expand their range. These documented changes in biodiversity require an adaptive approach to defining targets and implementing measures to achieve GES.

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Acknowledgments The Authors thank the regional and taxonomic experts who contributed to the clarification of doubtful species and records: Nikos Andreakis, Enrique Ballesteros, Jamila Ben Souissi, Ghazi

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Bitar, Cesare Bogi, Riccardo Brunetti, Mario Cormaci, Andrea Cosentino, Harlan Dean, Maoz Fine, Maria Cristina Gambi, Adriana Giangrande, Dani Golani, Menachem Goren, Cinzia Gravili, Jean-Georges Harmelin, Traudl Krapp-Schickel, Petar Kružić, Gretchen Lambert, Francesco Mastrototaro, Cristina Mazziotti, Henk Mienis, Frédéric Mineur, Luigi Musco, Marco

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Oliverio, Lidia Orsi-Relini, Stefano Piraino, Alfonso A. Ramos-Esplá, Stanley A. Rice, Fabio Rindi, Rosana Moreira da Rocha, Patrick Schembri, Adriano Sfriso, Marc Verlaque, Leandro M.

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Vieira, Johann W. Wägele, Helmut Zibrowius.

We thank the anonymous reviewers for their insightful and helpful comments. The research leading to these results has received funding from the European Community's Seventh Framework Program (FP7/20 07– 2013) under Grant Agreement no. 26 6 4 45 for the

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FIGURES CAPTIONS Fig. 1 – Map of the 23 countries facing the Mediterranean Sea: EU countries in pale yellow.

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Fig. 2 – Number of NIS by country, highlighting the different contribution of “established” species and “single records / extinct species”: species spotted only at one time, one place and with only one or very few individuals, or species known to be locally extinct. Fig. 3 – Cumulative number of established NIS (y-axis) for the three Italian sub-regions: Adriatic Sea, Ionian Sea and Sicily Straits, Tyrrhenian and Ligurian Seas (number of species in brackets). NIS are divided by vectors of introduction.

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Fig. 4 – Number of total NIS recorded in the Mediterranean Sea: (a) cumulative number; (b) number of records per decade. Fig. 5 – Dendrogram plot based on the similarity matrix of established NIS in the 11 Mediterranean countries with 50 or more NIS.

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Fig. 6 – Cumulative number of established NIS (y-axis) for selected countries with 50 or more NIS (Cyprus, Lebanon and Syria, not shown; number of NIS in brackets); by: (a) routes/vectors; (b) native origin; (c) taxa composition.

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Fig. 7 – Percentage of first Mediterranean records (blue) of the total number of established NIS in a country. Dimension of the pie charts is proportional to total number of established NIS.

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Israel Turkey Lebanon Egypt Italy Greece Cyprus France Tunisia Syria Spain

324 295 190 175 166 145 111 105 86 78 69

# First Mediterranean records 200 77 37 77 88 20 6 56 11 7 12

% First Mediterranean records 62% 26% 19% 44% 53% 14% 5% 53% 14% 9% 17%

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Table 1 – The number and percentage of earliest Mediterranean records of NIS in each Mediterranean country with 50 or more established species.

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Table 2 – List of NIS recorded in 10 or more Mediterranean countries. The country and year of first Mediterranean record and vector of introductions are reported. C= Culture; C, V= Culture, Vessels; Sc= Suez Canal; V= Vessels.

First record First record Vector (year) (country) Amathia verticillata (delle Chiaje, 1822) 1822 Italy V Pinctada imbricata radiata (Leach, 1814) 1874 Egypt Sc Brachidontes pharaonis (P. Fischer, 1870) 1876 Egypt Sc Cerithium scabridum Philippi, 1848 1883 Egypt Sc Hydroides elegans (Haswell, 1883) 1888 Italy V Halophila stipulacea (Forssk虱) Ascherson, 1867 1894 Greece Sc 1908 Greece Sc Lophocladia lallemandii (Montagne) F.Schmitz, 1893 Ficopomatus enigmaticus (Fauvel, 1923) 1919 Italy V Asparagopsis armata Harvey, 1855 1923 Algeria V Hemiramphus far (Forsskål, 1775) 1924 Israel Sc Siganus rivulatus Forsskål & Niebuhr, 1775 1924 Israel Sc Stephanolepis diaspros Fraser-Brunner, 1940 1924 Israel Sc Bursatella leachii Blainville, 1817 1930 Israel Sc Sphyraena chrysotaenia Klunzinger, 1884 1931 Israel Sc Fulvia (Fulvia) fragilis (Forssk虱 in Niebuhr, 1775) 1939 Egypt Sc Codium fragile fragile (Suringar) Hariot, 1889 1940 France C Callinectes sapidus Rathbun, 1896 1949 Italy V Crassostrea gigas (Thunberg, 1793) 1950 Tunisia C Saurida lessepsianus Russell, Golani, Tikochinski, 2015 1952 Israel Sc Siganus luridus (Rüppell, 1829) 1955 Israel Sc Oculina patagonica de Angelis, 1908 1966 Italy V Melibe viridis (Kelaart, 1858) 1970 Greece V Fistularia commersonii Rüppell, 1838 1975 Lebanon Sc Caulerpa cylindracea (Sonder) Verlaque, Huisman & Boudouresque, 2003 1990 Libya C, V Percnon gibbesi (H. Milne Edwards, 1853) 1999 Italy V Lagocephalus sceleratus (Gmelin, 1789) 2003 Turkey Sc

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