Floristic and Vegetation Changes on a Small Mediterranean Island over the Last Century

A synthetic and updated overview about the vascular flora and vegetation of the Island of Capo Passero (SE-Sicily) is provided. These data issue from two series of field surveys—the first carried out between 1997 and 2000, and the second between 2005 and 2019 and mostly focused on refining and implementing vegetation data. The current islet’s flora consists of 269 taxa, of which 149 (58%) are annual plants. The Mediterranean species are largely prevailing, 108 (40%) of which have a strictly Mediterranean biogeographical status. The comparison with a species list published in 1919 and updated in 1957 suggest that, despite the overall prevalence of anemochorous taxa, the vertebrate fauna represents an important vector for the plant colonization of the island, while the immigration of myrmechocorous taxa does not compensate the extinction rate. As many as 202 phytosociological relevés, 191 of which issue from original recent field surveys, enabled identifying 12 different plant communities. The comparison with a vegetation map published in 1965 suggests a strong reduction in dune habitats (2120 and 2210 according to EU ‘Habitats’ Directive 92/43), as well as a deep disruption in the succession typical of the local psammophilous vegetation series. In order to preserve rare, endangered and protected plant species (such as Aeluropus lagopoides, Cichorium spinosum, Limonium hyblaeum, L. syracusanum, Poterium spinosum, Senecio pygmaeus and Spergularia heldreichii) and to stop the ongoing habitat degradation, urgent and effective conservation measures should be adopted for this tiny, yet precious islet.


Introduction
Although they represent a small part of the emerged lands, islands host a remarkable portion of the global biological richness [1]. Indeed, the isolation of these lands and their ecosystems has not only favoured the processes of evolutionary divergence and endemism, but also offered refuge to organisms that are threatened or have disappeared elsewhere.
Among the circum-Sicilian islets, the Island of Capo Passero (SW-Sicily) stands out for having a prominent interest because, thanks to its easy accessibility, it has been targeted by numerous botanists. Its vascular flora was investigated for the first time during The Mediterranean chorotype was largely prevailing (124 taxa; 46%). Relevant was also the presence of the wide-Mediterranean (48; 18%) and (sub-)cosmopolitan taxa (34; 12%). The endemic component included two taxa restricted to SE-Sicily, Limonium hyblaeum and L. syracusanum, one restricted to SE-Sicily, Lampedusa and the Maltese Islands, Senecio pygmaeus, and two restricted to Sicily and southern Italy, Crocus longiflorus and Echium italicum subsp. siculum. The alien component, lumped into the category "other", is really negligible, being represented by five species which do not show any invasive behaviour locally (see Appendix A for details).
The ecological fingerprint of the vascular flora of the Island of Capo Passero, based on the Ellenberg's indicator values [39], suggested the intense solar radiation and the summer drought stress as major environmental drivers on the island, along with a neutral soil reaction and a relative lack of nutrients ( Figure 2).  . Seed dispersal strategies of the phanerogamic flora of Sicily (SIC) with that of the Island of Capo Passero (CP). The bar "+" refers to the species recorded in the present survey but not observed by Albo (1919Albo ( , 1957; "−" refers to the species recorded by Albo (l.c.) but not observed by us. Different letters indicate significant differences (p < 0.05).
The floristic differences with respect to the Albo's checklists [30,31] suggested that, despite the overall prevalence of anemochorous taxa, the vertebrate fauna represents an important vector for the plant colonization of the island and that epizoochorous plants have more chances to survive than endozoochorous. Additionally, the immigration of myrmechocorous taxa does not compensate the extinction rate ( Figure 3, first three columns).
The flora of the Island of Capo Passero hosts several taxa of high phytogeographic interest. The most interesting ones are briefly commented in the following paragraphs.

Aeluropus lagopoides (L.) Trin. ex Thwaites
This salt-tolerant geophyte usually grows in the gaps of chenopod scrub. Its distribution range includes the Mediterranean Islands, the Sahara and the Indian Subcontinent. Once widespread in Sicily, due to anthropogenic disturbance it currently occurs in few saltmarshes of western and southeastern Sicily. It features among the species assigned to Least Concern (LC) category according to IUCN criteria [40].

Cichorium spinosum L.
In Italy, this species is restricted to the SE-Sicilian coasts [31,41], which actually host the north-westernmost isolated population of this chamaephytic plant, quite common from sea level up to more than 1300 m a.s.l. in the East Mediterranean countries, but also widespread in Maltese Islands [42]. In the Island of Capo Passero, C. spinosum is localized in small areas along the rocky coast. Orsenigo et al. [40] reports this species as Endagered (EN) according to IUCN criteria.

Limonium hyblaeum Brullo
This salt-tolerant hemicryptophyte is considered to be endemic to SE-Sicily, where it is found only between Scoglitti and Capo Passero [43][44][45][46]. Quite surprisingly, it also occurs on the coastal rocky shores of Contrada Faraglione on the island Favignana (western Sicily), where it was already reported by Brullo [45] and was confirmed by S. Pasta and L. Scuderi (October 2004). As for the Island of Capo Passero, one single small population, represented by tiny individuals, was observed growing near the Spanish fortress. Although Orsenigo et al. [47] assigned the IUCN category Least Concern (LC) to this species, during recent times its extent of occurrence is rapidly shrinking, as the species is currently threatened with urban sprawl in most of its growing sites.

Limonium syracusanum Brullo
This chamaephyte is endemic to SE-Sicily [44,45]. More in detail, it is only found on the rocky cliffs along the Ionian coasts, between Penisola della Maddalena and Vendicari [41,43,48]. Never observed before on the islet, local population counts only a few individuals, localized in the extreme southern tip of the island. Orsenigo et al. [47] included this species among the Least Concern (LC).

Poterium spinosum L.
In Italy, this thorny shrub occurs in Calabria, Apulia and in one single locality of Sardinia [49], while SE Sicily hosts its main population, ranging from the sea level up to 600 m a.s.l.. Recently, Orsenigo et al. [40] confirmed the status Endangered (EN) for the Italian territory.

Senecio pygmaeus DC.
This therophyte is reported to be endemic to SE-Sicily, Maltese Archipelago and Lampedusa, growing near the coast, mostly in shallow soil pockets or along the sides of seasonal rock pools. Conti et al. [50] reported it as Endagered (EN) at the regional scale.

Spergularia heldreichii E. Simon & P. Monnier
The Island of Capo Passero hosts the only known population of this tiny therophyte in the whole Sicilian territory [38]. This salt-tolerant plant species, with a Mediterranean distribution, grows along the rocky coast, on small pools with sandy soil rich in salt, and subject to temporary flooding. Currently, no risk assessment has been carried out for this species.

Species Turnover, Population Trends and Landscape Evolution
Even if the list compiled by Albo presented a few identification pending issues (see notes in Appendix A for further details), the long time elapsed since his investigation on the Island of Capo Passero and the most recent ones raises some interesting considerations on the extent and direction of local species turnover and induced the authors to try to correlate these trends with local landscape dynamics. Several psammophilous species reported by Albo [30] have not been found anymore, such as Achillea maritima, Eryngium maritimum, Echinophora spinosa. This fact, together with the negative trend of some other coastal plants, such as Limonium hyblaeum and Calamagrostis arenaria subsp. arundinacea (=Ammophila arenaria) point out the severe effect of current disturbances (mostly linked to the seagull colony and seasonal tourism), to which have to be added also the sea currents and the wave motion that, in recent years, have determined the erosion of the sandy coast.
As already pointed out by Bergmeier and Dimopoulos [51], when the time lapse between floristic inventories is too large, like in our case, the available lists are often unable to 'capture' the ups and downs of local plant metapopulations. The risk of observation gaps is real: on the one hand, during the 30 years after the last census of Albo [31] as much as 48 taxa new to the islet have been recorded by Pirola [33] (8 additions), Galletti [35] (16 additions) and by Camatta et al. [36] (24 additions). On the other hand, many of these 'new entries' seem to have disappeared once again, as they have not been confirmed neither during the campaign carried out between 1997 and 2000 nor during last surveys (see Appendix A).
According to one of the key assumptions of island biogeography [52], colonization chances are higher-and consequently species turnover is more intense-on the small islets which are very close to large "species sources": this is the case of the tiny Island of Capo Passero, only 300 metres from the largest and plant species-richest island of the Mediterranean. Hence, it is not surprising if a relevant proportion of the taxa observed by Albo does not occur anymore. For the same reason, several species found for the first time by Cristaudo and Maugeri [37] (e.g., Hypericum triquetrifolium, Lemna minor, Vicia bithynica) have not been confirmed during the last survey, when some other taxa (e.g., Arenaria serpyllifolia, Cachrys pungens, Plantago afra, Spergularia rubra and Vicia villosa) were recorded for the first time (see Appendix A).

Current Vegetation Units
The cluster analysis of all vegetation relevés shows two main branches and 12 groups of plots belonging to 10 phytosociological classes ( Figure 4, Appendices B and C).
The first branch is characterized by scrub vegetation (cluster A1) and psammophilous communities together with the annual herbaceous communities (cluster A2); the second one (cluster B) includes the litho-halophilous vegetation linked to rocky coasts. The tallest vegetation found in the island is a maquis dominated by Chamaerops humilis and Pistacia lentiscus, referred to Pistacio lentisci-Chamaeropetum humilis (cluster 1, Table A2), which occurs in many other coastal sites of North-Western and South-Eastern Sicily [12,[53][54][55]. This maquis is often replaced by a phrygana-like shrubland dominated by the thorny cushions of Poterium spinosum on dry rocky stands with a shallow layer of soil, often representing a degradation serial stage of the coastal maquis. According to Minissale et al. [48], this community may be referred to the association Chamaeropo-Sarcopoterietum spinosi (cluster 2, Table A2). The most degraded stage of the vegetation in the inner areas is represented by a community dominated by Stipellula capensis and Asteriscus aquaticus belonging to Stipo-Bupleuretalia semicompositi order (cluster 3, Table A3), which is linked to uncultivated fields. Along the limestone rocky coast, in the small depressions covered by a thin silty-sandy layer, an annual halo-nitrophilous vegetation grows referable to Parapholido incurvae-Catapodietum balearici, often mixed with halophilous perennial species, as Limonium sinuatum and Limonium virgatum, and some annual plants of the class Stipo-Trachynietea distachyae (cluster 4, Table A2). Psammophilous vegetation only occurs in the few dune remnants near the southwestern shore of the islet. Across the landward gradient, the first

Changes Affecting Local Vegetation Patterns over Last Ha Century
Interesting clues on the recent evolution of the landscape are given by the comparison between the vegetation map of Pirola [34] with a new one based on aerial photographs dating back to 2019 (Table 1, Figure 5).  Pirola (1965) and the one produced by the authors combining the interpretation of recent aerial photos (2019) and field surveys. The list of the plant communities is shown in the legend included in each map. The corresponding habitats (according to European Directive 92/43 CEE) for each plant communities are listed in Table 1.
Thanks to repeated cross-checks supported by field surveys, the photointerpretation of the aerial photos enabled identifying 12 vegetation types, 10 of which represent habitats of community interest according to the EU 'Habitats' Directive 92/43 ( Figures A1 and A2).
The comparison of the two maps shows no significant differences in the area occupied by the vegetation. However, some variation in the area of occupancy of some vegetation units has been detected (Table 1). More in detail, the data show a strong shrinking of the vegetation of shifting dunes (Medicagini marinae-Ammophiletum arenarii) which decreased from 3 ha (8.7%) in 1965 to 0.05 ha (0.1%) in 2019, as well as of the Ononis ramosissima community (Centaureo-Ononidetum ramosissimae), which decreased from 3.6 ha (10%) to 1.8 (5.0%) ha. The cover of the most common plant community of the island, i.e., the dwarf maquis with Chamaerops humilis, has undergone a slight reduction, from 12.9 ha (36.0%) to 11.0 ha (31.0%). Inversely, the Poterium spinosum garrigue, together with the Chamaerops humilis maquis mixed with Poterium spinosum garrigue, increased from 2.4 ha (6.7%) to 5 ha (14.3%), as well as the dry grasslands (Stipo-Trachynietea distachyae) from 0.6 ha (1.7%) to 3.5 ha (10%).
The observed strong reduction in the dune system has been recorded in many other places along the Mediterranean coast [59][60][61][62][63]. These results highlight that human pressure directly and indirectly triggered the disruption of coastal dune systems, hugely affecting both the structure and the function of the local psammophilous plant communities. Therefore, the study case of Capo Passero Island, despite the modest size of the surveyed area, is a very representative example of how, within a few decades, seasonal trampling by tourists can destroy a dune system with direct negative consequences on the species and the communites/habitats linked to sandy shores. For the same reasons, some psammophilous species, recorded by Albo [30], such as Achillea maritima, Eryngium maritimum and Echinophora spinosa, have totally disappeared. This is in contrast to the conditions observed by Pirola [33], who depicted a vegetation transect (North-South section) indicating a well-preserved dune system in the southern part of the island.

Study Area
The Island of Capo Passero (latitude: 36 • 41 13 N; longitude: 15 • 08 56 E) has a surface of less than 36 ha and is located in front of the little town of Portopalo di Capo Passero, which corresponds to the south-easternmost corner of Sicily. The highest point of the island is 21 m. a.s.l., and currently hosts a lighthouse ( Figure 6). Despite its small size, the islet is characterized by many different types of sediments and rock outcrops [64,65]. From the most recent to the oldest one, these are: (1) recent sands and coastal dunes (Holocene), (2) limestones with Nummulites (Eocene) in the eastern part of the islet, (3) calcirudites with Rudistae (Upper Cretaceous) on northern sea cliffs and (4) base-rich vulcanites (Upper Cretaceous) along the eastern side.
The topography of the sea channel that separates the islet from Capo Passero, today c. 2.5 m in depth and 300 m in width, has been subject to continuous changes due to intense marine currents [66]. A long list of reports made by military engineers, maps, drawings, geographic treatises, sailor books testifie complex and long-lasting alternation of phases of closing and opening of this channel, partly driven by sea currents. After being isolated for about two centuries, around the mid 18th century the Island of Capo Passero was connected to the mainland by a thick sandy strip. Since then, the islet has been uninterruptedly separated from Sicily, as confirmed by numerous sources [29].
In order to prevent the incursions of pirates and to protect the south-eastern Sicilian coasts against them, the Spanish Government decided to build a fortress on the islet, whose construction was finished in 1635 [67]. Until mid 20th century, the islet was frequently visited by fishermen and people collecting the leaves of dwarf palms, whose fibers were used to produce several items (baskets, fans, hats, ropes, etc.). Nowadays, the Island of Capo Passero is uninhabited but it is home to a very large colony of yellow-legged seagulls (Larus michahellis Naumann), which induced a sharp increase in soil nitrogen content, significantly modifying local flora and vegetation as elsewhere in the Mediterranean [13].
Local climate is typically Mediterranean; based on the data from the nearby thermopluviometric station of Cozzo Spadaro (just 2.5 km from the study area), the mean annual temperature is 18.5 • C, while the mean annual precipitation, concentrated over the autumn and winter seasons, is 381 mm. According to the bioclimatic classification proposed by Rivas-Martiínez et al. [68][69][70], the investigated territory should be referred to the Mediterranean pluviseasonal oceanic bioclimate, with low thermomediterranean thermotype and dry ombrotype [71].

Data Sets and Data Processing
The collected plant specimens, were pressed in a plant press, dried on a plant dryer and stored in the Herbarium of the University of Catania (CAT). Specimens were identified following the second edition of the Flora d'Italia [72][73][74][75]. The floras by Fiori and Paoletti [76] and Fiori [77] were consulted as well, to ensure the best possibile interpretation of the plant names adopted in the lists published by Albo [30,31].
The family and the scientific name according to the Portal to the Flora of Italy [78] were assigned to each taxon, along with the following traits, extracted from the second edition of Flora d'Italia [72][73][74][75]: life form, chorotype, Ellenberg indicator values, pollination and seed dispersal strategies. The Pearson's χ2 test was used to compare some of the traits with those of the Sicilian flora and to get some clues on the variations occurred between the Albo floristic surveys [30,31] and the current vascular flora of the Island of Capo Passero. Statistical analyses were performed using R 4.0.3 [79] and the ggplot2 package [80] for data visualization.
The vegetation was sampled according to the phytosociological method [81]. The total amount of the vegetation data consisted of 202 phytosociological relevés, 191 of them issuing from recent field surveys carried out by the authors and 11 taken from literature [33]. For the numerical vegetation classification, the original Braun-Blanquet's sampling scale was transformed into ordinal scale according to van der Maarel [82] and a hierarchical clustering was performed by means of the PC-ORD 6 software. Clusters were interpreted basing on the syntaxonomic scheme by Mucina et al. [83] and other phytosociological papers from Sicily [10]. The detected vegetation units were then correlated to habitats of community interest following the Italian Interpretation Manual for the Habitats of Directive 92/43/EEC [84].
The current area of occupancy and distribution of the vegetation units was mapped using ArcGis 10.6 (ESRI Inc., Redlands, CA, USA). In order to perform a diachronic comparison between the past [34] and the current vegetation patterns, the interpretation of aerial images taken in 2019 (source: Google Earth) was validated by means of repeated field surveys.

Conclusions
This study has shown how the islet of Capo Passero has great floristic peculiarities and at the same time considerable vulnerability that can cause extinctions/decline of populations and reduction/alterations of habitats under stress. For this reason, it is important to plan and implement targeted conservation actions similar to what has been proposed for other small Mediterranean islands [4,85]. Already 50 years ago, considering the botanical interest of the Island of Capo Passero, Pirola [86] recommended its strict protection. The "Isola di Capo Passero" nature reserve was established on 16 May 1995 by decree of the Sicilian Regional Government. However, in 1998, after a long legal dispute following an appeal against the reserve made by the private owner of the island, the TAR (Regional Administrative Tribunal) canceled the protected area. Fortunately, the conservation measures of the Habitats Directive (EU 92/43) have allowed so far guaranteeing lasting protection of the island's naturalistic values. In fact, after the SCI proposal dating back to 1995 (ITA090001 "Isola di Capo Passero"), this Natura 2000 site was promoted as a Special Conservation Area (SAC) in 2017. Unfortunately, the lack of an encharged management body for this Natura 2000 site does not allow the implementation of active conservation and management policies (e.g., the regulation of visitors' access by creating of dedicated paths for seasonal tourists, who represent a serious threat for all the coastal habitats -especially 1210, 2120 and 2210-due to trampling and other kinds of disturbance, the control/eradication of the few occurring alien vascular plant species. This is a problem in common with all the Sicilian Natura 2000 sites which do not fall within the protected areas whose management is regulated by regional laws (e.g., nature reserves or regional parks) and is perfomed by public bodies and private NGOs.
The peculiar interest of this site for botanists is well documented since centuries (Pasta, submitted) and its paramount importance until present times its confirmed by recent inclusion among the Italian Important Plant Areas (IPA SIC17) according to Blasi et al. [87]. Moreover, the island and the nearby coast have an exceptional geological and paleontological interest, highlighted since the mid 19th century, for its fossil-rich (rudists, corals) outcropping limestones dating back to Cretaceous [64]. The historical and cultural sites by the island's castle and the Roman remains on the adjacent coast are no less important [88]. Unfortunately, all these natural and historical-cultural values are not protected adequately by local institutions, which instead have recently promoted some actions aiming at consolidating the rocky coast with concrete, damaging the coastal communities of the mainland promontory and deliberately introducing highly invasive alien plants such as Carpobrotus spp. This plant should be eradicated or monitored to avoid its introduction on the islet. Therefore, the authors suggest extending the limits of the SAC, so to include the Cichorium spinosum populations located in the promontory of Capo Passero ( Figure 6). This regionally rare and highly localized species characterizes two different habitats of community interest, i.e., the "Vegetated sea cliffs of the Mediterranean coasts with endemic spp." (Habitat code: 1240) and the "Sarcopoterium spinosum phryganas" (Habitat code: 5420). The enlargement of the Natura 2000 site, the designation of a qualified management body and the acquisition of the island as public ownership could guarantee a better management of this precious territory and the preservation not only of its naturalistic values but also the cultural heritage as a whole which originated, as in other Mediterranean sites, from with the harmonious balance between those values [89]. Although much still needs to be done, our map of plant communities ( Figure 5) is a solid basis for the management and monitoring of the habitats to be protected over time.