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The Native Distribution Range of the European Marine Non-Indigenous Species

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Aquatic Invasions (2018) Volume 13, Issue 2: 187–198 DOI: https://doi.org/10.3391/ai.2018.13.2.01 Open Access © 2018 The Author(s). Journal compilation © 2018 REABIC Review The native distribution range of the European marine non-indigenous species Konstantinos Tsiamis1,*, Argyro Zenetos2, Ivan Deriu1, Eugenio Gervasini1 and Ana Cristina Cardoso1 1European Commission, Joint Research Centre – Directorate for Sustainable Resources, Water & Marine Resources Unit, Ispra, Italy 2Hellenic Centre for Marine Research, Institute of Marine Biological Resources and Inland Waters, GR-19013 Anavyssos, Greece *Corresponding author E-mail: [email protected] Received: 14 July 2017 / Accepted: 24 December 2017 / Published online: 23 January 2018 Handling editor: Sarah Bailey Abstract In this study, we have performed a large-scale assessment on the native distribution range of the marine non-indigenous species (NIS) found in at least one of the European Seas (Mediterranean, NE Atlantic Ocean, Black, Baltic Sea). As a basis, we have used the most updated pan-European NIS inventory, provided by the European Alien Species Information Network. All taxonomic groups have been considered for this analysis, taking into account established NIS in European Seas (824 taxa in total). The vast majority of the European marine NIS have their native distribution in the Western and Central Indo-Pacific, being mostly associated with introductions into the Mediterranean Sea through the Suez Canal. However, this overall pattern is heavily influenced by the fact that 76% of all NIS primary introductions in Europe have been reported first from the Mediterranean Sea. A more detailed analysis revealed various patterns of the dominating native distributions of the primarily introduced NIS in Europe, depending on the European marine subregions where they have been initially introduced and their associated pathways. There seems to be a general decrease in NIS introductions in Europe, especially when it comes to NIS with native distribution in the Temperate Northern Pacific, although this trend should be treated with caution. The information provided in the current study can be useful for tailored management of specific primary pathways per marine subregion, supporting prioritization efforts. Key words: alien, pathways, trends, invasive, Mediterranean Sea, Black Sea, Baltic Sea, NE Atlantic, MSFD Introduction ments, such as the European Union Marine Strategy Framework Directive (MSFD) (EC 2008) and the Marine non-indigenous species (NIS) represent a Biodiversity Strategy (EC 2014). At the same time, significant risk to the receiving environments. They aiming to assist policy makers and environmental may exhibit invasive behavior and induce alterations managers in their decisions on prevention or miti- to ecosystems’ structure and functions, impede the gation actions, NIS have been thoroughly addressed provision of ecosystem services, and even result in by the scientific community, through the provision negative socioeconomic effects in coastal areas of recommendations for monitoring (e.g. Lehtiniemi (Wallentinus and Nyberg 2007; Molnar et al. 2008; et al. 2015), the revision of species inventories and Katsanevakis et al. 2014). New introductions of NIS spatial and temporal patterns (Zenetos et al. 2012, have been accelerated in recent decades by the rapid 2017; Katsanevakis et al. 2013b; Galil et al. 2016; globalization and increasing trends of human Ojaveer et al. 2016), pathways, gateways and their activities (shipping, aquaculture, fisheries, tourism, etc.) trends (Nunes et al. 2014; Galil et al. 2017), impacts (Boudouresque and Verlaque 2005; Katsanevakis et (Katsanevakis et al. 2014, 2016), and biological traits al. 2013a). of the most widespread species (Cardeccia et al. 2016). By 2013, at least 1,369 NIS have been reported Specific focus has been given to the Mediterranean from all European and contiguous seas (Katsanevakis Sea, the most invaded marine region of the world, et al. 2013b). Due to the threats they pose, European with at least 821 multicellular NIS (casuals included) NIS are targeted in a series of legislative instru- reported by early 2017 (Zenetos et al. 2017). 187 K. Tsiamis et al. Several studies have addressed the native distri- NIS with unresolved taxonomic status). Species that bution range (possible origin) of the European are predominantly freshwater but which might also marine NIS, but most of them have examined this appear in oligohaline environments (i.e. with salinity issue only at regional or country level. Some examples < 5 psu) were also excluded from the current study. include the native distribution of NIS of the Baltic Consequently, 824 established NIS have been consi- Sea (Leppäkoski et al. 2002), Belgium (Kerckhof et dered in the present paper (Appendix 1). The al. 2007), Germany (Gollasch and Nehring 2006), Taxonomic classification (Kingdom, Phylum, Class, British Isles (Minchin et al. 2013), Israel (Galil 2007), Order and Family) of each NIS followed WoRMS Italy (Occhipinti-Ambrogi et al. 2011), and Greece (2017). (Zenetos et al. 2009). In addition, the CIESM atlases The EASIN data encompass the four main European provide information on the native distribution of NIS Seas: the Black Sea, the Mediterranean Sea, the NE belonging to four taxonomic groups in the Medi- Atlantic Ocean, and the Baltic Sea. To have full terranean Sea, namely Fish, Crustacea, Mollusca, coverage of the four Seas surrounding Europe, Macrophytes, but with no detailed analysis (Galil et EASIN contains NIS reported from the whole Medi- al. 2002; Golani et al. 2002; Zenetos et al. 2004; terranean Sea, including also North African and Verlaque et al. 2015). Surprisingly, there has not Near East Mediterranean countries. EU overseas been any study so far providing a large-scale assess- territories (including the Outermost Regions, e.g. the ment of the native distribution of all NIS across all Macaronesia Sea) were not considered. European Seas. We have assigned the known native distribution In this study, we investigate the native distri- to each NIS of the EASIN dataset based on the bution of NIS recorded in at least one of the main scientific literature, AquaNIS Editorial Board (2015) European Seas: the Mediterranean, NE Atlantic and WoRMS Editorial Board (2017). Afterwards, Ocean, the Black and the Baltic Seas. All taxonomic the native distribution of each NIS was classified groups of NIS have been considered for this analysis. based on the global marine biogeographic realms In addition, primary pathways of introduction are proposed by Spalding et al. (2007), slightly modified examined in relation to each main native distribution for the aims of our study. To this end, we have split area of NIS. Time trends of species introductions in the realm “Temperate Northern Atlantic” into 3 relation with the prevailing native distribution areas distinct realms: a) the “Temperate Northwest are also investigated. Atlantic”, including the provinces “Cold Temperate Northwest Atlantic” and the “Warm Temperate Methods Northwest Atlantic”; b) the “European Seas”, which include the provinces “Northern European Seas”, For the present analysis, we have used the pan- “Mediterranean Sea”, “Black Sea”, and the ecoregion European inventory of NIS provided by the “South European Atlantic Shelf”; and c) the European Alien Species Information Network “Saharan Upwelling” (see also Figure 1). In case (EASIN – Katsanevakis et al. 2012) and updated up the native distribution of a species covers more than to March 2017 (EASIN Catalogue version 5.6), one marine realm, multiple realms were assigned to based also on the recent work by Zenetos et al. that species. For few NIS the native distribution is (2017). EASIN is a dynamic inventory that is conti- unknown (13 taxa; see Appendix 1). nuously updated to follow the latest scientific Based on an extensive revision of the information findings about new NIS species in Europe and their found in EASIN and the scientific literature, we have status. The latest version of the EASIN database analyzed the information on primary introduction contains 1,411 NIS reported from European marine pathways for each marine NIS in Europe, i.e. the waters, including all taxonomic groups, from bacte- pathway(s) related to the first arrival of a NIS in ria to mammals. Species with a native distribution in Europe. Pathways followed the classification scheme at least one European Sea but with alien range into proposed by CBD (2014). A certainty score was other(s) have been also included in our analysis, given to each assigned pathway for every NIS, based hereafter referred to as NIS with “European origin”. on the scheme proposed by Katsanevakis et al. Only established NIS have been taken into consi- (2013a), and slightly modified as follows: deration. To this end, we have excluded casual (i.e. High certainty (score = 3): there is direct evidence NIS not established in Europe, found only once or of a pathway; this is the case e.g. for most intentional twice), cryptogenic (i.e. species with no definite introductions (e.g. Release in Nature: fishery in the evidence of their native or introduced status) and wild – including game fishing) and in many cases of questionable species (i.e. NIS with insufficient Lessepsian immigrants (Corridor: interconnected information or new entries not verified by experts or waterways/basins/seas) when there is direct evidence 188 Native distribution of European marine non-indigenous species Figure 1. Native distribution
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