Alien flora in Calabria (Southern Italy): an updated checklist

An updated checklist of the Calabrian alien vascular flora is presented. By way of field, bibliographic, and herbarium research, we recorded 382 alien taxa (representing almost 14% of all regional flora), of which 371 are angiosperms, nine gymnosperms, and two ferns. In relation to the state of spread, the majority of alien species are casual (207 taxa; 54%), followed by naturalized (127; 33%) and invasive (48; 13%), these last include four on the list of Union Concern, sensu Regulation (EU) no. 1143/2014. The most represented families are Asteraceae (39 taxa) and Poaceae (39). Among genera, Amaranthus (nine taxa), Prunus, Euphorbia, and Oxalis (seven taxa) make up those with the greatest number of taxa. A total of 21 taxa were reported for the first time, three of them are new to the European flora (Camptosema rubicundum, Musa ×paradisiaca and, only for continental Europe, Ipomoea hederacea), two to the Italian peninsula (Pelargonium graveolens, Schinus terebinthifolia) and 16 to the Calabrian flora (Aeonium arboreum, Asparagus asparagoides, Aspidistra elatior, Bidens sulphurea, Catalpa bignonioides, Citrus ×aurantium, Crassula ovata, Cucurbita ficifolia, Dimorphotheca ecklonis, Graptopetalum paraguayense subsp. paraguayense, Kalanchoë laxiflora, Nicotiana tabacum, Phytolacca dioica, Portulaca umbraticola, Talinum paniculatum, Tecomaria capensis). In terms of residence status, there are 291 neophytes (76%), 73 archaeophytes (19%), and 18 regional aliens (5%); neophytes are the most represented group (45 out of 48) among invasive taxa. Concerning life forms, the two most abundant groups are therophytes (30.1%, 115 taxa) and phanerophytes (29.6%, 113 taxa). Regarding habitats, 72% of alien taxa occur in artificial (199 taxa, 52%) and agricultural habitats (75 taxa, 20%). The majority of alien taxa are native to the Americas (159; 41.6%), numerous aliens also originated in Asia (76; 19.9%) and Africa (56; 14.7%). The majority of taxa were introduced for ornamental purposes (55%). Over the past decade, alien taxa in the flora in Calabria have increased from 190 to the current 382 taxa. While this trend could be linked to some extent to increasing awareness of the problem of alien species and the increasing intensity of research over recent decades, it is also most probably due to new introductions resulting from the globalization that relentlessly affects the whole planet.


Introduction
Biological invasions are one of the greatest threats to biodiversity in the world, second only, in terms of severity, to the destruction of natural habitats (Lawler et al. 2006;Pyšek et al. 2020). The annual rate of first records worldwide has increased since 1800, and 37% of these have occurred over the last 44 years (Seebens et al. 2017). Alien species are recognized as a significant component of human-caused environmental global change, which also affects the conservation of biodiversity and the function of invaded ecosystems (Weber 2003;Pyšek et al. 2004;Richardson and Pyšek 2006). Alien species can affect the quality of habitats available to other species and consequently the ecosystem services provided Gutiérrez 2017; Vilà and Hulme 2017;Castro-Diéz et al. 2019). Many studies ascertained and documented that alien species, especially invasive ones, can also cause considerable socio-economic and health damage (Richardson et al. 2000;Bacher et al. 2017).
Alien plants are becoming an important component of wild floras and are a real challenge for current and future environmental and habitat management (Maes 2013;Pyšek et al. 2020;Gigante et al. 2018;Raposo et al. 2021).
Checklists are essential for studies on biogeography and provide an important tool for biodiversity conservation (Perrino and Signorile 2009;Perrino et al. 2013;Musarella et al. 2018;Wong and Joling 2021). Alien plant checklists are critical to understanding plant invasion in many places around the world (Celesti-Grapow et al. 2009, 2010, 2016Galasso et al. 2018a;Lazzaro et al. 2020;Viciani et al. 2020) Datasets on the floristic state, biological attributes, and the geographic distribution of alien species are significant tools for understanding the invasiveness of alien species (Pyšek et al. 2002(Pyšek et al. , 2004Haq et al. 2021).
The total number of alien plants in the European flora, currently estimated at around 6000 taxa, has tripled in the last half-century and will continue to increase through to 2050 (Lambdon et al. 2008;Pyšek et al. 2017;Seebens et al. 2017Seebens et al. , 2021. Many studies on alien plants are available for Italy on a national or regional scale (Stinca et al. 2017(Stinca et al. , 2021Rosati et al. 2020;Galasso et al. 2018a) reported 1741 alien species for the Italian territory, of which 236 are invasive; 20 of these species are included in the EU list according to Regulation 2016/1141, of 13 July 2016 and 2019/1262 of 25 July 2019 (European Commission 2019). This checklist has been updated by several other works up to the present (Galasso et al. 2018b(Galasso et al. , c, 2019a(Galasso et al. , b, 2020a(Galasso et al. , b, 2021a. Furthermore, Lazzaro et al. (2019) proposed a list of 96 alien species that should be included in the Italian national list according to EU Regulation 1143/2014.
Calabria, located at the southern end of the Italian peninsula in the centre of the Mediterranean Sea, has been identified by historical and environmental data as a refuge area during Quaternary for several plant taxa, very important for their conservation (Médail and Diadema 2009). Calabria is one of the regions with the highest number of endemic plant taxa (Pignatti 1994). Indeed, after the two large Italian islands of Sicily and Sardinia, Calabria is the third richest region in endemics (Peruzzi et al. 2014).
Various authors have dealt with alien flora in Calabria (Viegi et al., 1974;Celesti-Grapow et al. 2009;Galasso et al. 2018a). Moreover, information on the regional alien flora is available in certain Italian checklists and floras Pignatti 1982Pignatti , 2017aPignatti ,b, 2018Conti et al. 2005;Pignatti et al. 2019). More recently, Bartolucci et al. (2021) provided an updated overview of native and alien vascular flora of Italy, with details on occurrences at national and regional administrative level.
For Calabria, there is a number of recent contributions mainly thanks to the research of this working group Musarella et al. 2019Musarella et al. , 2020Musarella 2020;Rosati et al. 2020;Laface et al. 2020;Stinca et al. 2021), including many new records, that improved knowledge on alien flora in this region. Yet, there a comprehensive analysis of the regional alien vascular flora of this region is missing.
The aim of this study is to present an updated checklist of alien vascular flora within the Calabrian region (Southern Italy), with information on the origin, distribution, and invasion status of alien taxa and their habitats. This new and updated data should contribute to filling the knowledge gap on alien species in the Mediterranean region and Southern Europe to the same degree as the better-known alien flora of Central and Northern Italy and temperate Europe.

Study area
Calabria is the southernmost region of the Italian Peninsula (Fig. 1). It has an area of 15,081 km 2 with a population of 1,877,728 inhabitants (ISTAT 2021), corresponding to an average density of 126.6 inhabitants/km 2 .
Calabria is a narrow peninsula in the central Mediterranean basin, approximately 250 km long, surrounded on three sides by the sea, with a coastal development of 715 km. The region is crossed from north to south by a series of mountainous reliefs at varying altitudes between 1,400 m and 2,200 m a.s.l., which together constitute the Calabrian Apennines, a continuation of the southern Apennines. The territory is mostly hilly (49% of the area), there are few plains (9%), and large areas are mountainous (42%). As regards land use in Calabria, the following Land Cover Corine categories (ISPRA 2019) are indicated: level 1-artificial surfaces (3.7%), level 2-agricultural areas (48.6%), level 3-forest and seminatural areas 48.3% (of which 31% are forested), level 4-wetlands (0.003%), level 5-inland water bodies (0.3%). Annual precipitation varies from 600 to 1800 mm, and mean annual temperature from 12 to 19 °C. The prevailing bioclimate is the Mediterranean pluviseasonal oceanic type, widespread from sea level to ~ 1000-1100 m a.s.l., at higher altitudes, it is the oceanic temperate type (Pesaresi et al. 2017).
The native flora of the Calabria region is estimated at 2,768 native taxa (species and subspecies) ( Bartolucci et al. 2018Bartolucci et al. , 2021, with additional 342 aliens reported by previous studies (Galasso et al. 2018a;Bartolucci et al. 2018Bartolucci et al. , 2021.

Data sources and terminology
The critical analysis of bibliographic information, herbarium specimens, and observation and field collections carried out in this study made it possible to update the checklist of alien vascular flora in Calabria. The dataset for the current checklist originates from a preliminary list of Italian alien species based on Celesti-Grapow et al. (2010), Galasso et al. (2018a), and Bartolucci et al. (2018), updated with the above-mentioned literature for Italy and Calabria in particular and integrated with additional and updated information, field collections and surveys. Collected specimens are preserved at the Herbarium of the Mediterranean University of Reggio Calabria (REGGIO; acronym according to Thiers 2021). Historical records (species no longer registered for 50 years, probably casual alien that have not established), and doubtful records (doubtfully occurring in the region, probably reported by mistake or confused with other species), are listed in the Online Resource 1 but not analyzed in this study.
Each species record is supplemented with data on taxonomy, life form and growth type, presence status, invasion and residence status, habitats, and frequency. The nomenclature of taxa follows Galasso et al. (2018a) and Bartolucci et al. (2018), that of the families the APG system (Stevens 2001 onwards).
Data relating to the geographical distribution, origin, and introduction pathway come from several online databases on alien species (CABI 2021;EPPO 2021;GBIF 2021;ISSG 2021; Portal to the Flora of Italy 2021; POWO 2021). Taxonomic assignment of alien plants to genera and families to allow for comparison with native species follows Bartolucci et al. (2018Bartolucci et al. ( , 2021. Introduction pathways were assessed by distinguishing the following categories: ornamental, forestry, agricultural and unknown (species without information on the purpose of introduction).
We classified the invasion status of alien plant species according to Richardson et al. (2000Richardson et al. ( , 2011 and Pyšek et al. (2004) to distinguish casual (alien plants that may occasionally reproduce outside cultivation without forming self-replacing populations, their persistence depends on repeated introductions), naturalized (alien plants that sustain self-replacing populations and reproduce without direct human intervention from seed or vegetative parts capable of independent growth), and invasive (a subset of naturalized plants with the potential to spread over a large area in natural or man-made habitats, thanks to high reproductive efficiency and their long-distance dispersion ability from parent plants). We also recognized regional aliens that are native to other parts of Italy but alien in Calabria (according to Bartolucci et al. 2018). Plants kept only in cultivation are not included in this study.
Taxa with uncertainty as to whether they are native or alien are considered cryptogenic (Carlton 1996). They are listed in the checklist (Online Resource 1) but not considered in this study.
The following habitat groups were distinguished according to the Corine Land Cover system (CEC 1994): artificial surfaces (constructed, industrial and other artificial habitats, ruderal sites, and linear infrastructure), agricultural areas (regularly or recently cultivated agricultural, horticultural and domestic habitats), natural and seminatural habitats. The latter were divided into grasslands, riparian habitats, shrubland, wetland (including water bodies), woodland, and coast. The distribution of taxa among the different habitats was inferred from literature and from field observations on the frequency of occurrence. When a taxon is present in more than one habitat, the prevailing one is reported.

Statistical analysis
The processed data were subjected to statistical analysis. To prove that the observed values fit the expected frequencies, the variables were arranged in the form of standardized contingency tables and the chi-square test was carried out. All analyses were performed with Microsoft Excel® spreadsheet software.
The genera with the highest number of alien taxa are Amaranthus (nine taxa), Prunus, Euphorbia and Oxalis (seven), Bidens (six), Vitis, Cyperus, and Solanum (five taxa). Most genera include only one taxon. The richest genera include weed species or species of agronomic interest.

New aliens to calabrian flora
The field research carried out in this study has identified several new alien vascular taxa for the flora of Calabria. A complete list of these taxa is given in Online Resource 2 with complete information on collection locations and their environmental conditions. Three taxa are new to the European alien flora
Compared to native flora, alien taxa are overrepresented among phanerophytes and under-represented among hemicryptophytes, the differences being highly significant (P < 0.001). There were no significant differences for the other categories of life forms (Fig. 4). The higher frequency of phanerophytes results from the introduction and widespread use of trees and shrubs for ornamental purposes, such as Acer negundo, Amorpha fruticosa, Austrocylindropuntia subulata, Schinus molle, Sesbania punicea, but also in forestry (Acacia saligna, Robinia pseudacacia, Populus ×canadensis, Eucalyptus camaldulensis, E. occidentalis) and in agriculture (i.e., crops such as Ricinus communis, Vitis rupestris, Opuntia ficus-indica).
The distribution of phanerophytes and nanophanerophytes compared for casual vs. naturalized taxa, including invasive, was significantly different; taxa of this life form were recorded as casuals with lower frequency than expected and with higher than expected among naturalized. For the other life form categories the differences were not significant (Fig. 5).

Discussion
The data reported by several scholars highlights a hyperbolic increase of alien species in Calabria, especially in recent years. The records of alien plant taxa to Calabrian flora increased from just 12 in 1974(Viegi et al. 1974, to 163 (Pignatti 1982), 190 in 2009by Celesti-Grapow et al. (2009, 267 of Galasso et al. (2018a), 284 (Pignatti 2017a,b;Pignatti et al. 2019), and, finally, 342 taxa were recorded by Bartolucci et al. (2021). Moreover, Conti et al. (2005) reported 119 invasive and naturalized taxa for Calabrian flora, excluding casual ones, as previously recorded by other authors. Our survey yielded 382 taxa for alien Calabrian vascular flora. According to Bartolucci et al. (2018Bartolucci et al. ( , 2021, the native regional flora of Calabria includes 2,786 taxa (including species, subspecies and hybrids), therefore, approximately 14% of the regional flora is made up of alien taxa. The rapid increase in alien taxa is due to new introductions, as a result of globalization, which affect the entire planet, producing biotic homogenization (Stohlgren et al. 2011). However, there is an awareness of the problem of alien species and an increase of studies in recent decades.
The comparison with other Mediterranean countries, such as Algeria (211 alien plant taxa) (Meddour et al. 2020), Turkey (340 taxa) (Uludağ et al. 2017) or Greece (343) (Arianoutsou 2010a), highlights the abundance of alien taxa (including casual, naturalized and invasive aliens) in Calabrian flora, considering that these Mediterranean territories are much larger. This data is confirmed by the density of alien taxa in Calabria (log taxa/log km 2 of area), which is 0.62, and ranks Calabria among the Mediterranean territories with the highest levels of invasion; the corresponding value for Greece is 0.50, for Algeria 0.36 and Turkey 0.43. Compared to other Italian regions, the number of alien taxa in Calabria corresponds to other less populated agricultural regions, such as Puglia (202.2 inhabitants/km²; 361 alien taxa) and Abruzzo (117.6 inhabitants/km²; 350), far from the industrialized and densely populated regions of the north of Italy, such as Lombardy (417.6 inhabitants/ km²; 776) and Veneto (264.6 inhabitants/km²; 618) (ISTAT 2021; Galasso et al. 2018a).
The richest families of Calabrian alien flora are Asteraceae, Poaceae, Fabaceae, and Solanaceae, which are also dominant in other European alien floras (Pyšek et al. 2002;Lambdon et al. 2008;Galasso et al. 2018a) and globally . Poaceae, Fabaceae, and Asteraceae are also the largest families in the native Mediterranean flora (Heywood et al. 2007). On the other hand, the Solanaceae family is less represented in native Calabrian flora but is mainly an extra-European plant family with many taxa introduced as cultivated plants (Tutin et al. 1972).
The genus Amaranthus is the most representative in Calabrian alien flora, among other genera, as well as in several countries of the world Galasso et al. 2018a;Weber et al. 2008;Lambdon et al. 2008). In addition to this genus of North American origin, there are also others, such as Bidens, Cyperus, and Solanum, comprising mainly urban and agricultural weeds (Lambdon et al. 2008).
The prevailing life form among aliens in Calabria are therophytes and phanerophytes that have approximately the same percentage; overall, woody species (phanerophytes and nanophanerophytes) are more abundant than therophytes. This pattern is different from the native flora of Calabria, where the most represented groups are therophytes and hemicryptophytes (Fig. 4). The preponderance of phanerophytes/ nanophanerophytes among aliens is a common character in invasive floras in various territories due to the preference of gardeners for ornamental trees (Crawley et al. 1996). In the alien flora of other Mediterranean territories, such as Greece (Arianoutsou et al. 2010b) and Sardinia (Podda et al. 2012), a common feature is the dominance of phanerophytes/nanophanerophytes and therophytes that appear best suited to overcome the long dry seasons typical of the Mediterranean bioclimate (Wagner et al. 2017). They occupy different niches, and their success in colonizing new territories is based on them possessing different strategies -phanerophytes cope with water scarcity through their architecture, while therophytes avoid the dry season (Allen 2001). Alien taxa are present in Calabria in artificial, comprising human-disturbed and urban sites, and agricultural habitats, but a significant percentage occur in natural and seminatural habitats. This is quite alarming because it shows that about a third of alien taxa grow in natural environments that are vulnerable due to the anthropic pressure linked to urbanization.
Most Calabrian alien taxa are of neotropical origin. These are thermophilous taxa coming from South America that are favoured by the Mediterranean bioclimate that affects a large part of the region, up to about 1000 m of altitude. An important group of alien plants also comes from Asia; these are plants of warm environments, too, that easily spread in the Mediterranean territories. Some studies show that global warming favours the spread of alien tropical or subtropical taxa in Europe, mainly introduced into gardens for ornamental purposes (Dullinger et al. 2017). The majority of alien taxa are introduced as ornamental plants, including in Calabria, and especially in urban areas, which represent preferential routes for invasive taxa; favoured by global warming, such species can easily spread to the surrounding areas (Géron et al. 2021).

Conclusions
This study highlights a progressive and constant increase in alien taxa in the vascular flora of Calabria and provides a baseline for further studies on the management of invasive species and invasion ecology. The habitats located at lower altitudes (0-200 m a.sl.m.) are most threatened by the spread of alien taxa; road and railway infrastructures are the main ways of spreading alien plants. On the other hand, waterways and disturbed humid environments also contribute to the maintenance and invasions of alien taxa (See ESM 2). Further investigations are needed to better quantify the damage caused by invasive species to natural ecosystems and habitats.
Most of the new entries are represented by plants that have escaped from gardens, confirming the importance of ornamental plant cultivation as a source of such introductions.
Any future solutions to contain the problem depend not only on the tools made available by the legislator and on the interventions implemented by the administrators of local authorities but also on the ability of researchers and administrators to find technical solutions and make citizens aware of the rules and behaviour needed, especially in nursery fields (Caddeo et al. 2020).

Acknowledgements
The authors are very grateful to Monika Mojtova for the first linguistic review of the text, to Laura Celesti-Grapow, the other anonymous referee and the "Alien Floras and Faunas" Section Editor Petr Pyšek for their invaluable help to improve the manuscript. The final version of the paper was reviewed by Edward Parker.
Funding Open access funding provided by Università degli Studi Mediterranea di Reggio Calabria within the CRUI-CARE Agreement.
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