Introduction
Urbanization and climate change encourage the invasion and spread of exotic plant species (Salinitro et al. 2019). In particular, several alien species have recently been reported in Italy (Sciandrello et al. 2016, Galasso et al. 2018, Musarella 2020). Many of them belong to the Malvaceae Juss. s.l, in fact, ca. 43% of the taxa within this family reported in Italy are non-native (Portal to the Flora of Italy 2022).
The family Malvaceae includes ca. 250 genera and 4200 species distributed mainly in the tropical regions of the world (Simpson 2019). Phylogenetic studies of this family show its division into nine subfamilies (Chase et al. 2016). Following this classification, the genus Sida L. falls within the tribe Malveae J. Presl belonging to the Malvoideae Burnett subfamily. The genus Sida L. was validly described by Linnaeus (1753), and it is one of the most diversified genera of the Malvaceae. This genus includes ca. 250 taxa, and its native array ranges from the Tropics to N America (POWO 2021), and from a taxonomical point of view, it is very complex due to its great changeability. Moreover, these species also usually grow in areas with a high degree of human intrusion. The genus Sida is distinguished from other related genera by two morphological features: calyx often 10-ribbed, and schizocarp fruits with 5-14 one-seed mericarps, muticous to prominently aristate (Fryxell 1997).
Duringfield surveys in the northeast region of Sicily, we discovered several individuals of an unknown Sida representative mainly associated with urban areas. The plant was identified as Sida rhombifolia L. through literature and herbarium research. This species, widely distributed in the tropical, sub-tropical and warm temperate regions of the world (Holm et al. 1997), has not previously been reported for the Italian flora. Its real native range is unknown, but it is probably attributable to the Paleotropics (Verdcourt 2004). It is mainly known for its medicinal uses in tropical and subtropical areas worldwide (Ajeet et al. 2018), where it shows a potential for invasiveness (Randall 2001). Generally, S. rhombifolia is a common weed in synanthropic stands from sea level to 2,000 m a.s.l., particularly along roadsides and urban areas, as well as in gardens, pastures, abandoned farmland and cultivated fields (Smith 1981). Sometimes, it also colonizes scrubs, open slopes, stream sides, seasonally flooded surfaces and degraded forest areas, while it does not grow in closed forests or tall scrublands (Vattakaven et al. 2016). It constitutes a serious nuisance for agricultural lands, pastures, and native grasslands (Reddy 2011).
Until today, the only known species belonging to this genus in Italy was Sidaspinosa L., which is reported as a casual alien species (Galasso et al. 2018). In addition, S. rhombifolia is a taxonomically controversial species, which belongs to Sida section Sida. Different authors attributed many binomials and now some of them are considered as autonomous taxa within the S. rhombifolia complex. This new alien species to Italy was already reported in other countries of Europe and the Mediterranean area. It is reported as casual and ephemeral species in the Czech Republic (Pyšek et al. 2012), France (Tison and de Foucault 2014), Great Britain (Clement and Foster 1994), Netherlands and Belgium (Verloove and Vandenberghe 1995), while it is indicated as naturalized in Croatia (Milović et al. 2010), Portugal (Webb 1968) and Spain (Pavia and Nogueira 2006). It is categorized as “not established” in Lithuania, Sweden, and Norway, while its status is unknown in Ukraine and Denmark (Valdés 2011, NOBANIS 2021). Besides, in the Mediterranean area S. rhombifolia is reported as native to Egypt (Boulos 2000).
The aim of this paper is to analyze the morphological, ecological and chorological features of the Sicilian populationof S.rhombifolia (the only population currently known in Italy). Additonally, the invasive behavior in and potential impacts on Italy have been assessed.
Material and methods
This investigation was conducted between August 2014 and April 2021 in the Peloritani Mounts, (Northeastern Sicily) based on literature data and morphological analysis of living material collected during fieldwork. Careful surveys of the Italian literature were carried out to find existing records of the species in Italy (Pignatti et al. 2017-2019, Galasso et al. 2018). The specimens have been kept in the herbaria of the University of Catania and Messina (CAT and MS; herbarium acronyms follow Thiers 2020). Taxonomic identification was performed according to Pavia and Nogueira (2006), Tambde et al. (2016) and Pignatti et al. (2017-2019), while the nomenclature was compiled following Bartolucci et al. (2018), Galasso et al. (2018) and subsequent updates reported in the Portal to the Flora of Italy (2022). In addition, many herbarium sheets of S.spinosa and S.rhombifolia were carefullyexamined for the correct identification of the species. Morphological measurements were carried out on 10 specimens for each area using Zeiss Stemi 500 stereoscope with Zen 2.5 lite software. The stands where the species was discovered were reported in a distribution map, developed using QGIS tools (QGIS.org 2021). The vegetation in which this species was found was studied following the Braun-Blanquet approach (Braun-Blanquet 1964) and the nomenclature of syntaxa follows Mucina et al. (2016). Moreover, possible impacts and invasive behavior were analyzed using the EPPO prioritization method scheme for invasive alien species (Branquart et al. 2016). This prioritization process, broadly, aims to compile a list of invasive alien plants that have grown in the assessment region, and to identify which of these should be prioritized for a Pest Risk Analysis (PRA, see EPPO 2019).
Results
Sida rhombifolia L., Sp. Pl. 2: 684, 1753 (Fig. 1) Lectotype – Herb. Linnean No. 866.3 (LINN), designated by Rodrigo 1944.
Synonyms – Diadesma rhombifolia (L.) Raf., New Fl. 1: 41, 1836; Malva rhombifolia (L.) E.H.L.Krause, Deutschl. Fl. Ed. 2, 6: 238, 1902; Napaearhombifolia (L.) Moench, Methodus 621, 1794; Sida alba Cav., Diss. 1: 22, 1785; Sida andicola Gand., Bull. Soc. Bot. France 71(5–6): 632, 1924; Sida compressa Wall. Cat. N. 1866, 1824; Sida hondensis Kunth, Nov. Gen. Sp. 5: 260, 1822; Sida insularis Hatus, J. Jap. Bot. 35: 360, 1960; Sida pringlei Gand., Bull. Soc. Bot. France 71: 631, 1924; Sidarhombifolia subsp. Insularis(Hatus) Hatus, Fl. Ryukyus 846, 1976; Sida rhombifolia subsp. Rhombifolia Borss. Blumea 14: 195, 1966; Sida ruderata Macfad., Fl. Jamaica 1: 80, 1837; Sida unicornis Marais, Kew Bull. 38: 42, 1983.
Species description from Sicilian material
Perennial herb or semi-woody shrub up to 1–1.5 m tall. Stems erect, terete, green or purplish, many-branched, with sparse stellate hairs when younger and almost glabrous when older. Leaves alternate, slightly dimorphic, rhomboid to elliptic and with stellate hairs on both surfaces of the young branches without flowers, narrower and with stellate hairs only on the abaxial face on the flowering stems. Blade elliptic to rhomboid, 1.5–5.5 × 1–3 cm, serrate and crenate towards the top and entire towards the base, apex obtuse. Leaves with petiole 0.2–0.5 cm long, couple of stipules, 3–5 mm long, not different, linear to filiform. Calyx campanulate, pubescent, with triangular sepals, 0.4–0.7 × 0.2–0.4 cm. Flowers solitary or gathered in small groups, axillary, on slender pedicel, 2 to 3 cm long, jointed above the middle. Corolla with 5 petals partially fused together, slightly longer than calyx, pale yellow, 0.5–1 × 0.5–0.7 cm. Schizocarp, flattened or almost globular, from greenish (immature) to brownish (mature), 0.4–0.5 cm long, with peduncle 1.4–2.8 cm long; mericarps 8–10, dark brown to black, wedge-shaped, 0.3–0.4 cm long, with two vertical ribs and a pair of retrorse awns on the top, 0.5–1 mm long (Figs. 2,3).
Taxonomic remarks concerning S. rhombifolia
According to several authors (Fryxell 1988, Tambde et al. 2016), S.rhombifolia represents a species complex with a great morphological variation, including many taxa treated at a specific, subspecific or varietal level. Indeed, the taxonomy of this complex species is quite disputed (Aguilar et al. 2003), and the proposed classification is often very different according to the various geographical areas, lacking an overall treatment of the entire group in all its range. The specimens collected in the northeast of Sicily can be referred toS.rhombifolia L., showing leaves with an indumentum of minute sessile stellate hairs, and serrate margins at the apex, as well as dehiscent mericarps provided with 2 prominent apical awns. Finally, it should be pointed out that the only other species of the Sidagenus present in Italy is S.spinosa, first reported for western Sicily by Romano (2004). These two species are easily distinguished for several features, and based on our measurements and bibliographic data, the following analytical key is provided:
1a. Plant 2–6 (–10) dm tall, stems with 1 or 2 spines at the base of petioles, leaf blades narrow-ovate to oblong or elliptic, 5–7 mericarps with 2 awns 1–1.5 mm long....................................................................... Sida spinosa
1b. Plant 10–15 dm tall, stems without spines at the base of petioles, leaf blade elliptic to rhomboid, 8–14 mericarps with 2 awns 0.5–1 mm long ............................................................................................ Sida rhombifolia
Distribution and ecology of S. rhombifolia in Italy
Sidarhombifolia wasfound in five localities of the Peloritani Mounts (Northeastern Sicily), along the coastal belt between Furnari and Rometta, near Messina (Fig. 4). It mainly colonizes disturbed sites not far from the sea, at an altitude of 0-140 m a.s.l., such as roadsides, abandoned quarries and uncultivated areas, which are characterized by high levels of nitrates and a certain amount of moisture. From a phytosociological point of view, this species plays a dominant role in the community characterized by several nitrophilous annual species with a summer-autumn cycle, such as Digitaria sanguinalis (L.) Scop., Eleusine indica (L.) Gaertn., Euphorbia prostrata Aiton, Setaria verticillata (L.) P.Beauv., Dittrichia viscosa (L.) Greuter, Foeniculumvulgare Mill. Subsp. Vulgare, Rubus ulmifolius Schott, Geranium molleL.,MalvasylvestrisL.,Oxalispes-capraeL.,Portulacaoleracea L., Sixalix atropurpurea (L.) Greuter & Burdet, Sonchus tenerrimus L., Sorghum halepense (L.) Pers., Symphyotrichum squamatum (Spreng.) G.L.Nesom, Verbena officinalis L., Vicia villosa Roth, Xanthium strumarium L. (Tab. 1).
Therefore, these aspects should be referred to the Amarantho-Digitarietum sanguinalis Pignatti 1953 (Digitario sanguinalis‐Eragrostietea minoris Mucina, Lososová & Šilc 2016), anthropogenic vegetation described by Pignatti (1953) for the Venetian plain and recently reported by Viciani et al. (2020) in the checklist of the alien-dominated communities in Italy. Besides, S. rhombifolia sometimes forms dense monodominant vegetation or mixed communities with R. ulmifolius, unlike other parts of continental Europe where it is very ephemeral and mature individuals are seldom seen (Verloove and Vandenberghe 1995, Milović et al. 2010). In Sicily, it is locally well established and exhibits high coverage with a growing number of individuals, according to our observations in the period 2014-2020 (Fig. 5). The stands of S.rhombifolia distributed in the northeast of Sicily are represented by several individuals (ca. 50–100 for each stand), and due to the awned seeds, the species mainly spreads by adhering to clothing and animals (Smith 2002). The introduction of S. rhombifolia in Sicily was almost certainly accidental, probably due to seeds carried on vehicles in an area of trade such as the Messina Strait or it could have come from the nursery activity specialized in the trade of exotic species, since the first finding was made in an area with a high human presence.
According to Pyšek et al. (2004), the invasion status of the species can be considered in Italy as naturalized. Besides, the EPPO protocol (Branquart et al. 2016) was performed on S.rhombifolia. The result of the assessment (evaluation of spread, impacts, and uncertainty degree) is shown inTab. 2.
Discussion
This new record of S. rhombifolia for Italy seems to not show a high invasive potential of the species, despite its increasing spread in the Mediterranean Europe territories in recent years. This species in Sicily has not yet colonized habitats with a significant ecological value. However, in the future, based on its ecological requirements and ongoing climate changes occurring in Italy, it might invade natural environments of this area, such as grasslands (Habitat code 6220), and the wide pebbly bottoms of seasonal waterways locally knownas“fiumare”(Habitatcode 3290). Sidarhombifolia together with other invasive species reported from the Northeastern part of Sicily, such as Euphorbia hypericifolia L., Ailanthusaltissima (Mill.) Swingle., Lantanacamara L., Boerhavia coccinea Mill., Digitaria ciliaris (Retz.) Koeler, Opuntia ficus-indica (L.) Mill. (Sciandrello et al. 2016, Galasso et al. 2020), could represent a serious threat for many natural habitats in this area, hosting narrow endemic species (Sciandrello et al. 2019, Brullo et al. 2021).
Furthermore, the occurrence of numerous other sites with similar ecological characteristics makes expansion foreseeable in the coming years, not only in the Messina area, but also in other parts of Sicily, considering the high invasive potential of this species observed in numerous geographical areas (Rejmánek 2016, Kuswantoro et al. 2020). As highlighted by Steel et al. (2008), based on mathematical models, global warming could lead to a significant invasive potential of the species, even in non-tropical areas and in those with a Mediterranean climate.
In conclusion, it would be desirable to monitor the species in the Sicilian territory, in order to supervise the expected spread in the above mentioned habitats so as to limit alteration of the floristic and structural composition of these environments.
Specimina visa:
Sidarhombifolia L.–Portugal: Azores, 1846, T. Hunt s.n. (BR0000013473679); India: Tamil Nadu Peninsula Indiae Orientalis Madras, 1867, Wight 166 (K000659356); Cameroon: Koum, 25 August 1974, MM Bosch Geerling & L.V.P. Lavieren 5169 (YA0053739); Usa: Sumter County, S Side of Cane Savannah, 5 air mi SE of downtown Wedgefield, 23 August 2019, J.B. Nelson &D.P. Ferral s.n. (USCH0053519); FairfieldCounty, 2.8 road miles N of downtown, Ridgeway, 6 September 2019, J.B. Nelson s.n. (USCH0058773); Italy: Sicily: Barcellona Pozzo di Gotto, lungo il margine dei Caselli autostradali, 12 m, 22 August 2014, A. Crisafulli & A. Soldano s.n. (MS); Rometta, 5 m, 21 February 2016, A. Crisafulli s.n. (MS); ibid., 20 December 2020, S. Cambria& G.Tavilla s.n. (CAT); Valdina nel lago grande, 16 m,3 January 2017, A. Crisafulli s.n. (MS); ibid., 16 m, 13 November 2020, S. Cambria s.n. (CAT).
Sida spinosa L.–Italy: Sicily: Misilmeri, contrada Incorbina (Palermo), September 2001, S.Romano s.n. (PAL); Brazil: Monte Corcorado, January 1818, without collector (W00693489; Sergipe, Capela, RVS Mata do Junco, Mata Atlantica, May 2012, L.A.Gomes et al. s.n. (NY); São Sebastião da Vitória, 10 May 2014, M.T.R. Costa s.n. (RB00947655); Colombia: Tocaima, November 1932, E. Pérez Arbeláez 2447 (COL000141171); Usa: North Carolina, Poplar Branch Township, 21 September 2018, T. Holdsclaw s.n. (NCU659548).