Alien Plant Invasions in Mediterranean Habitats: an Assessment for Sicily

Biol Invasions https://doi.org/10.1007/s10530-021-02561-0 (0123456789().,-volV)( 0123456789().,-volV) ORIGINAL PAPER Alien plant invasions in Mediterranean habitats: an assessment for Sicily Riccardo Guarino . Milan Chytry´ . Fabio Attorre . Flavia Landucci . Corrado Marceno` Received: 9 November 2020 / Accepted: 1 May 2021 Ó The Author(s) 2021 Abstract Levels of plant invasions in different longer flowering period than the native species. The habitat types were assessed in several regional studies, investigated habitats differed strongly in their level of but few of them were from the Mediterranean. Here invasion by alien species, ranging from 0 to 15.6% of we compare the levels of vascular plant invasion aliens of all species recorded. Most of the habitats across habitats and plant communities of Sicily. We were colonized by very few alien species or com- used a large dataset of plant species presences/ pletely lacked them, except for sandy coasts, natu- absences in vegetation plots to analyze the invasion rally-disturbed riverbeds, and synanthropic habitats. It patterns across habitats considering biogeography, life must be noted, however, that the number of alien form and phenology of alien plants. Vegetation plots species occurring in a given habitat does not relate to were classified based on the EUNIS classification of the severity of the impact of invasion in that habitat. European habitats. The invasiveness of each species Some habitats are invaded by few (or single) species, was expressed in terms of its absolute and percentage which attain a high cover, transforming the whole frequency. Representation of different life forms and ecosystem. The habitat-based approach proved to be phenological patterns was compared between alien suitable for evaluating the habitat specificity and and native species. The fidelity of alien species to frequency of alien species at a regional scale, individual habitats was calculated using the phi improving the capacity for risk assessment in different coefficient. Our analysis shows that annual and woody ecological contexts. species are the most represented life forms in the alien flora of Sicily and that alien species tend to have a Keywords Alien species Á Biogeographical status Á Flowering season Á Life form Á EUNIS Á European vegetation archive R. Guarino (&) Department of Biological, Chemical and Pharmaceutical Sciences and Technologies, University of Palermo, Palermo, Italy e-mail: [email protected] Introduction M. Chytry´ Á F. Landucci Á C. Marceno` Department of Botany and Zoology, Faculty of Science, Some authors have considered Mediterranean ecosys- Masaryk University, Brno, Czech Republic tems less prone to invasion than temperate ecosystems as a result of the long history of interactions between F. Attorre Department of Environmental Biology, Sapienza the environment and humans (Di Castri 1989; Que´zel University of Rome, Rome, Italy 123 R. Guarino et al. et al. 1990) and summer-drought stress, which used to designate an integral unit comprising ecolog- prevents the establishment of non-adapted plants ical functions and species assemblages (Morrison and (Garcia-Serrano et al. 2009). This is consistent with Mathewson 2015), as it happens in the EUNIS habitat recent syntheses that show generally lower numbers of classification adopted in the European nature conser- alien species in the Mediterranean than in temperate vation policies (Rodwell et al. 2018). In this sense, the Europe, based on national inventories of alien floras invasiveness of an alien species is determined not only (Lambdon et al. 2008b), Atlas Florae Europaeae grid by its habitat preferences but also by context-specific maps (Ronk et al. 2017) or standardized plot sampling processes and interactions between biotic communi- of corresponding habitats in the Mediterranean and ties and their invaders (Lambrinos 2002; Evangelista temperate cities (Kalusova´ et al. 2019). However, et al. 2008; Crosti et al. 2016). recent studies suggest that disturbance (Dimi- Regional studies comparing the levels of plant trakopoulos et al. 2017), human population density invasion across Mediterranean habitats and plant (Malavasi et al. 2014), habitat fragmentation (To- communities are uncommon, most of them performed maselli et al. 2012), climate change (Gritti et al. 2005), on the Iberian Peninsula (Vila` et al. 2007; Chytry´ et al. global trade (Hulme 2004), and ornamental horticul- 2008; Gonza´lez-Moreno et al. 2014). Therefore, we ture (Pretto et al. 2012) may lead to an accelerating extend this approach eastwards to test whether the trend of biological invasions also in the Mediterranean patterns documented previously have a more general region (Sanz-Elorza 2006; Celesti-Grapow et al. 2010; validity across the Mediterranean Basin. Celesti-Grapow and Ricotta 2021), mainly by plant We focus on Sicily, the largest Mediterranean species arriving from climatically similar regions of island. Due to its long-lasting human history and the world (Cao Pinna et al. 2021). central location in the Mediterranean Basin, Sicily Mediterranean islands also seem to be less invaded represents an ideal study area to explore alien plant than areas of continental Europe, as indicated by invasions patterns. Although Sicily’s alien vascular qualitative observations of their flora (Dal Cin flora is well known (Galasso et al. 2018a, b, c), the D’Agata et al. 2009; Podda et al. 2010; Puddu et al. frequency and abundance of alien species within 2016). However, islands tend to be more prone to habitat types have never been assessed. invasions than mainland regions (Lonsdale 1999), and Since vegetation cover is a primary attribute in this pattern was also observed in the Mediterranean EUNIS habitat identification (Gigante et al. 2016; (Gimeno et al. 2006; Celesti-Grapow et al. 2016). The Rodwell et al. 2018) and vegetation plots offer a good reasons include a higher probability of the occurrence measure of species percentage frequencies in different of unsaturated communities, a lower competitive habitats (Guarino et al. 2018), we used vegetation-plot ability of native species (Hulme 2004) and more data from Sicily to answer the following questions: (1) intense human pressure, notably in summer along the What is the affinity of alien species to specific habitats coast, in lowlands and riparian habitats (Hulme et al. at a fine-scale? (2) Which biogeographical regions 2008). Also, the exposure of Mediterranean islands to contributed the most frequent alien vascular plants to biological invasions may have accelerated in recent Sicily and the study habitats? (3) Which are the most years as it happened elsewhere. For instance, Camarda frequent life forms of the alien vascular plants in Sicily et al. (2016) report on the naturalization of 72 new and in the study habitats? (4) Are there any differences alien plant species never observed before in Sardinia. in the flowering time of alien and native plants? The distance from the mainland, size and shape of the Mediterranean islands can influence their vulnerabil- ity to alien plant invasion (Domina and Mazzola Methods 2011). Still, some studies (Vila` et al. 2010, 2011) suggest that biological invasions in Mediterranean Study area insular ecosystems are no exception to the general rule that levels of invasion are context-dependent and Sicily and its offshore islets are recognized as one of habitat-specific (Traveset et al. 2008). the biodiversity hotspots in the Mediterranean Basin The term ‘‘habitat’’ originates from a species- (Me´dail and Que´zel 1999). Sharp topographic (Cata- specific concept (Kirk et al., 2018), but it is frequently lano 2004), edaphic (Fierotti 1997) and climatic 123 Alien plant invasions in Mediterranean habitats: an assessment for Sicily (Bazan et al. 2015) contrasts make this island one of Macaronesian Vegetation Information System the most environmentally heterogeneous Mediter- (SIVIM, EU-00–004; Font et al. 2012) and VegItaly ranean territories. The diversity of the Sicilian flora (EU-IT-001; Landucci et al. 2012). and vegetation is due to the complex geomorphology Vegetation plots were classified using the classifi- of the island (Carbone et al. 2018) and its palaeo- cation expert system for EUNIS habitats (EUNIS-ESy geographic history, making Sicily an excellent exam- version 2020–06-08; Chytry´ et al. 2020). Habitat types ple of the full range of common Mediterranean within groups A (marine, in our case coastal salt- vegetation types (Guarino and Pasta 2017). marshes), C (aquatic) and H (sparsely vegetated) were Its central location made Sicily a major pathway of classified to the types accepted in the European Red human migration and cultural, economic and ethnic List of Habitats (Janssen et al. 2016) because these crossroads. Although palaeontological and palaeogeo- groups of habitats were not yet subjected to the graphic data do not exclude the possibility of a Middle revision of the EUNIS system. Unclassified plots and Pleistocene peopling (Sineo et al. 2015), the human those assigned to multiple habitats were discarded. presence in Sicily has been unequivocally continuous Only habitats represented by at least 34 plots across since 14,000 years ago (Mannino et al. 2012). During the whole dataset were retained for data analysis. In the long history of human habitation, plant assem- some cases, similar habitats not reaching the minimum blages have been shaped by human activity (Tinner number of plots were merged. This happened in the et al. 2016). Many alien vascular plants were intro- case

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