Exotic Ants (Hymenoptera, Formicidae) Invading Mediterranean Europe: a Brief Summary over About 200 Years of Documented Introductions Sociobiology

Exotic ants have emerged as a relevant topic worldwide because of their remarkable impacts on native ecosystems and human activities. A first regional overview is given on the dozens of exotic ant species recorded in Mediterranean Europe since the end of the 19 th century. About 40 exotic ant species, belonging to 17 genera and originating from 5 different biogeographical realms, are currently believed to be established in this region. The genera Nylanderia and Tetramorium are those hosting the larger proportion of species, while the Afrotropical realm is the prevalent source of taxa. According to the available data, France, Greece, Italy and Spain all host a high number of exotic species, which has increased at a dramatic rate during the last decades. On the other hand, Mediterranean countries on the Eastern part of the Adriatic Sea appear to be almost empty of exotic ants, perhaps due to both a lesser number of introductions and a lack of targeted investigations. Neighboring countries of the region do not necessarily have more species in common than those geographically distant. Very little is known on the intra-Mediterranean or intra-Palearctic introduction processes which probably occurred prior to the 19 th century and on their influence on the current species distribution. The vast majority


Introduction
Introduction of exotic species is a global problem affecting human activities and whole natural ecosystems. Exotic ants represent only a very tiny fraction of global ant diversity (McGlynn, 1999), and most of them tend not to spread outside the human-modified habitats where they first arrive (Holway et al., 2002). Nonetheless, many others have a significant ecological impact and may become invasive, even outside anthropogenic habitats, sparking serious concern and attention from researchers worldwide (Holway et al., 2002;Lach et al., 2010). Five ant species are considered among one hundred worst alien species in the world, representing almost one third of the terrestrial invertebrates of the list Abstract Exotic ants have emerged as a relevant topic worldwide because of their remarkable impacts on native ecosystems and human activities. A first regional overview is given on the dozens of exotic ant species recorded in Mediterranean Europe since the end of the 19 th century. About 40 exotic ant species, belonging to 17 genera and originating from 5 different biogeographical realms, are currently believed to be established in this region. The genera Nylanderia and Tetramorium are those hosting the larger proportion of species, while the Afrotropical realm is the prevalent source of taxa. According to the available data, France, Greece, Italy and Spain all host a high number of exotic species, which has increased at a dramatic rate during the last decades. On the other hand, Mediterranean countries on the Eastern part of the Adriatic Sea appear to be almost empty of exotic ants, perhaps due to both a lesser number of introductions and a lack of targeted investigations. Neighboring countries of the region do not necessarily have more species in common than those geographically distant. Very little is known on the intra-Mediterranean or intra-Palearctic introduction processes which probably occurred prior to the 19 th century and on their influence on the current species distribution. The vast majority of the species that are currently established in the region are either restricted to indoor habitats or outdoor anthropogenic habitats, fewer of them were able to colonize semi-natural or natural habitats and very few are recognized as serious pests.
produced by Lowe et al. (2000). Eradication of these species may unfortunately prove to be extremely difficult to achieve if populations are well-established (Holway et al., 2002;Hoffmann et al., 2011;Hoffmann et al., 2016).
In Europe, alien terrestrial invertebrates represent one of the most numerous groups of organisms introduced, and are mostly represented by insects (Roques et al., 2009). An exponential increase of the number of established species is currently being witnessed, and it is expected to continue in relation to globalization and expanding commerce (Roques et al., 2009). Climatic conditions made it so that only very few exotic ant species have become established outside heated buildings in Central and Northern Europe (Seifert, 2018). On the contrary, Mediterranean Europe has seen dozens of Section Animal Biology, Department of Biological, Chemical and Pharmaceutical Sciences and Technologies (STEBICEF), University of Palermo, Italy REVIEW exotic ant species establishing during the last 200 years in non-heated and even undisturbed natural ecosystems. The Mediterranean basin was recognized as one of the twenty-five biodiversity hotspots worldwide (Myers et al., 2000), and it is host to a rich ant fauna (Borowiec, 2014). Its invasion by the exotic Argentine ant, Linepithema humile (Mayr, 1868), one of the worst invasive aliens in the world according to Lowe et al. (2000), attracted alone dozens of studies, making L. humile the single most-studied ant species of the entire region (e.g. Giraud et al., 2002;Espadaler & Gómez, 2003;Gómez et al., 2003;Rey & Espadaler, 2004;Blancafort & Gómez, 2005;2006;Carpintero et al., 2005;2014;Jacquiery et al., 2005;Oliveras et al., 2005a;2005b;Wetterer & Wetterer, 2006;Abril et al., 2007;2010;Blight et al., 2009;2010;2012;Roura Pascual et al., 2009a;2009b;2010;Pons et al., 2010;Estany-Tigerström et al., 2010;Abril & Gómez, 2011;Angulo et al., 2011;Diaz et al., 2014;Centorame et al., 2017;Queiroz & Alvez, 2018). Displacement of native ants and significant changes in the native ant communities are among the most commonly documented consequences of ant invasions, but in many cases notable effects have been also reported in regard to other invertebrates, vertebrates and plants (Holldöbler & Wilson, 1990;Holway et al., 2002;Lach et al., 2010).
Currently, records of exotic species in Mediterranean Europe come from a large number of different published studies, including only very few updated syntheses at national level (Salata et al., 2017;Blatrix et al., 2018). No comprehensive look at the exotic ants issue at regional or continental levels has ever been taken, while the same was done in case of organisms whose ecological impacts have been much less documented (e.g. Nentwig, 2015).

Materials and methods
A 'practical' definition of Mediterranean Europe was given: the sum the European territories of all the countries of the Mediterranean region (see Myers et al., 2000 for the region geographic definition), excluding the microstates (e.g. San Marino), was considered (Fig 1). Following this definition, Albania, Bosnia and Herzegovina, Croatia, France, Greece, Italy, Montenegro, Portugal, Slovenia, Spain and Turkey are the nations whose territories are included at least in part.
These territories are not entirely characterized by a Mediterranean climate, especially in the case of France, whose vast majority is not. However, since the non-Mediterranean areas are usually not witnessing significant exotic ant invasion processes, the European territories of these nations are simplistically considered in their entirety instead of being divided in Mediterranean and non-Mediterranean areas. Moreover, in order to facilitate the distinction of exotic from native species, especially in regard to the intra-Mediterranean exotics, all the Mediterranean islands that belong to these countries were excluded with the exceptions of the very large Corsica, Crete, Sardinia and Sicily. The hundreds of smaller islands of the Mediterranean basin are in fact mostly littleknown from a myrmecological standpoint, and only very few were studied with particular regard to the exotic species (e.g. the Balearic Islands by Gómez & Espadaler, 2006).

Results and Discussion
A total of 40 different species, belonging to 17 genera and four subfamilies, originating from five biogeographical realms, were found to be currently considered to be present as exotic in Mediterranean Europe and recorded since the second half of the 19 th century. The prevalent genera are Nylanderia Emery, 1906 and Tetramorium Mayr, 1855 with 5 species each. The count also includes three provisionally unnamed morphospecies whose identity still needs to be ascertained (Brachymyrmex sp. from France and Nylanderia spp. from Italy -see Blatrix et al., 2018;Schifani & Alicata, 2018) and a dubious identification (Tetramorium cf. simillimum (Smith, F., 1851) from France -see Blatrix et al., 2018).
Four relatively well-studied countries (France, Greece, Italy and Spain) are characterized by four relatively rich lists of exotic species (Table 1, Fig 1), and similar incremental trends across the decades (Fig 2). Although some of the more recently introduced species may not manage to establish durable populations (thus lowering the '2000' peaks in Fig 2), the vast majority of them are already known as very successful tramp species across other regions of the world (see Antmaps). France is distinguished among the four countries by its comparatively smaller number of exotic species established outdoor (only about 27% of the list, while 73% to 90% in the others), most-likely due to the fact that only a very small part of its territory belongs to the Mediterranean climatic region. In these four countries, the exotic species number represent approximately around 4.5-7.5% of the entire myrmecofauna present. The Afrotropical realm is always the most important source of species, while the rest of the species origins are mostly divided between the Palearctic, Indomalayan and Neotropical realms (Fig 3). Such pattern is significantly different compared to the one at a global scale (McGlynn, 1999). It is important to note that many of these species are currently widespread across the globe due to human introductions, so that they may have easily been introduced to Europe from areas outside their native range. Five exotic species are actually shared by these four countries (Hypoponera punctatissima (Roger, 1859), Linepithema humile, Monomorium pharaonis (Linnaeus, 1758), Paratrechina longicornis (Latreille, 1802), Tetramorium bicarinatum (Nylander, 1846)), while four others are present in only three of them (Lasius neglectus Van Loon, Boomsma & Andrasfalvy, 1990, Nylanderia jaegerskioeldi (Mayr, 1904, Pheidole indica Mayr, 1879, Strumigenys membranifera Emery, 1869). In Greece, the presence of L. neglectus was initially supposed to be incorrectly recorded due to misidentification with the native L. turcicus Santschi, 1921(Borowiec & Salata, 2012. Later, the same authors reported to have collected material of both species (Borowiec & Salata, 2013;Salata & Borowiec, 2018) and the situation remained unresolved as the two may be conspecific (Borowiec & Salata, 2017a). In any case, L. neglectus was listed as a nonexotic species in Greece lately (Salata et al., 2017;Salata & Borowiec, 2018).
The Sørensen-Dice coefficient was used in order to compare the list of these four species-rich countries ( Table 2). Very different results were obtained if the comparison was made between all the exotic species of each country, only between those species that managed to establish outdoor or only between those able to colonize non-urban habitats. In any case, the coefficient values that were obtained do not show any strong biogeographic pattern of colonization: neighboring countries do not necessarily show a higher degree of similarity than geographically more distant countries do, suggesting that species often spread through multiple introduction events.

Korlevic, 1886
Nylander, 1856 Bolton, 1987Mantero, 1908Zimmermann, 1934Collingwood & Prince, 1998Bračko, 2000Santschi, 1925 Aktaç  Table 1. Exotic ant species established or seemingly established in France (Corsica, mainland), Greece (Crete, mainland, Peloponnese), Italy (mainland, Sardinia, Sicily) and Spain (mainland). The first confirmed record of the species in each country is presented on the right of the species name. Species that have been found outdoors are marked in yellow, species that have also colonized areas outside urban contexts are marked in red. (Latreille, 1802) Nylander, 1856Kugler, 1988Süss, 1979Espadaler & Collingwood, 2000 Pheidole anastasii (Emery, 1896) Bernard, 1968 Pheidole  Table 1. Exotic ant species established or seemingly established in France (Corsica, mainland), Greece (Crete, mainland, Peloponnese), Italy (mainland, Sardinia, Sicily) and Spain (mainland). The first confirmed record of the species in each country is presented on the right of the species name. Species that have been found outdoors are marked in yellow, species that have also colonized areas outside urban contexts are marked in red. (Continuation) No exotic species is currently recorded in Albania and Bosnia and Herzegovina. Such condition of these countries, confirmed in the aforementioned relatively recent checklists, may partly be explained by a lack of targeted searches but may also be partly related to the recent history of the former Yugoslavia, and certainly requires further investigations. No species were found to be considered exotic in any of the four large islands included in this study while at the same time being considered native in the respective country's mainland or vice-versa.

Paratrechina longicornis
Some species seem to differ in their invasion success across different countries examined: the same species may be restricted to indoor habitats in a country, be present outdoor but only in anthropogenic habitats in another, and to be present in semi-natural or even natural-habitats in a third one. Such differences can be related to many factors, including environmental aspects and priority effects in the area where the species were introduced, genetic variability and consistence of the introduced population and time-related effects, since many invasion processes are known to be subject to a variety of lag phenomena (Crooks, 2005). While only a small portion of the exotic ants listed in Tab. 1 are considered significantly threatening to semi-natural and natural ecosystems in the Mediterranean basin (Lasius neglectus and Linepithema humile above all), some others have aroused different levels of concern in different countries. For example, Tetramorium bicarinatum, first recorded in the Mediterranean region by Bondroit (1918), is globally considered a low threat (Wetterer, 2009), and usually restricted to indoor areas. However, it has lately started to be reported in outdoor urban contexts in Spain (Reyes & Espadaler, 2005), Italy (Borowiec & Salata, 2015;Schifani & Alicata, 2018) and Greece (Salata et al., 2017). Moreover, in Greece it was also considered by Salata et al. (2017) among the three exotic species that displace native ants in the areas they occupy.
In general, the few species that successfully invaded large areas of outdoor habitats in all the countries considered in this study are mostly distributed in areas characterized by a strictly Mediterranean climate (e.g. Blatrix et al., 2018). A significant exception is that of Monomorium carbonarium (Smith, F., 1858), whose presence is mostly distributed along the Atlantic coast of France, while mostly along the Mediterranean in Iberia (Miravete et al., 2013).
Given the long history of human activities and commerce across the Mediterranean basin, many cases of old historical or pre-historical introductions have been detected for both animal and plant species. However, intra-Mediterranean or intra-Palearctic introductions of ants, usually much less obvious to detect than these of ants from other continents or latitudinal regions, actually represent a mostly unexplored topic. Some cryptic species belonging to the Tapinoma nigerrimum complex and the Tetramorium caespitum complex were only recently recognize as exotic in some or all of the countries in this study after the latest taxonomic advances Wagner et al., 2017). However, the time of their introduction is unknown and thus they were excluded from the present analysis. Another issue is that for a number of other Mediterranean species, there is no precise knowledge about where their native range ends and where the exotic range begins. For example, the status of Cardiocondyla mauritanica Forel, 1890 in Sicily is currently dubious (Schifani & Alicata, 2018): it is considered as an exotic species in Greece (Salata et al., 2017) and Spain (Reyes & Espadaler, 2005;Reyes-López et al., 2008), while as likely native to North Africa (Wetterer, 2012). In Sicily, it is found in both natural and anthropogenic habitats, and many species appear to be naturally present in both Sicily and North Africa (Alicata & Schifani, 2019). Monomorium subopacum (Smith, F., 1858) was considered as exotic in Greece by Salata et al. (2017), while it is usually considered native in the Mediterranean region, however it was removed in a more recent list by the same authors (Salata & Borowiec, 2018).  Aphaenogaster splendida (Roger, 1859) may be exotic at least in some parts of the Italian territory (Schifani & Alicata, 2018) and was only recently treated as an exotic species in Crete (Salata & Borowiec, 2018). Still, the definition of its native range remains unclear. Similarly, Monomorium monomorium Bolton, 1987 is considered as exotic in Greece (Salata & Borowiec, 2018) but it is usually considered native in Mediterranean Europe (e.g. Antmaps). Hypoponera eduardi is usually considered native to the Mediterranean, but it is regarded as exotic in Greece (Salata et al., 2017) and Turkey (Kiran & Karaman, 2012), although Lapeva-Gjonova and  treat it as a rare species attributing conservation value to an area of Turkish Thrace. Another example can be provided by some forms related to Lepisiota frauenfeldi (Mayr, 1855), whose scattered distributions across the Mediterranean basin may suggest some of these populations are introduced, especially given the vast exotic range attained by L. syriaca (André, 1881) in Greece according to Salata et al. (2017) or the recent quick invasion of the Canary Islands by L. frauenfeldi cf. kantarensis (Forel, 1911)  . Molecular data may allow to shed light into this complex and mostly unexplored issue in the future, as in the case of Anochetus ghilianii Forel, 1915 in Southern Spain (Jowers et al., 2015).

Conclusions
The numerical increase of exotic ant species established in Mediterranean Europe during the last decades is impressive, and so is also the increasing rate at which they continue to be introduced. Nonetheless, other countries around the world are already dealing with much higher numbers of exotic species (e.g. Deyrup et al., 2000). The Balkan countries bordering the Adriatic Sea make an interesting exception in the region, which requires further investigation. It is impossible to predict which species are going to be successful invaders when they arrive, and the ongoing climate change further complicates this equation (Bertelsmeier et al., 2015). Moreover, existing data do not allow to attempt predictions on which species are going to be the next to be introduced in the region, especially that similarity between exotic ants assemblages is not always greater between neighboring countries. While our understanding of invasive ants has tremendously increased over the last decades, long-term effects and dynamics of the invasive populations are little-known since they are just starting to be observed (e.g. Tartally et al., 2016). Our knowledge also remains extremely scarce on those successful ants' introductions that have most likely occurred across the Mediterranean basin in historic and pre-historic times, and on their possible role in shaping the current faunas. The number of species which have caused serious damage and concerns in Mediterranean Europe remains relatively low for the time being. Still, the current situation is concerning for the equilibrium and management of natural and anthropogenic ecosystems in the future.