ACTA BOT. CROAT. 81 (2), 2022 159 Acta Bot. Croat. 81 (2), 159–167, 2022 CODEN: ABCRA 25 DOI: 10.37427/botcro-2022-013 ISSN 0365-0588 eISSN 1847-8476 First record of Sida rhombifolia L. (Malvaceae) for Italian flora: taxonomical and ecological investigation Salvatore Cambria1, Alessandro Crisafulli2, Gianpietro Giusso del Galdo1, Rosa M. Picone2, Adriano Soldano3, Saverio Sciandrello1, Gianmarco Tavilla1* 1 University of Catania, Department of Biological, Geological and Environmental Sciences, via A. Longo 19, I-95125 Catania, Italy 2 University of Messina, Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, Via Stagno d’Alcontres, 98100 Messina, Italy 3 Largo Brigata Cagliari, 6, 13100 Vercelli, Italy Abstract – Sida rhombifolia L. (Malvaceae) has been reported for the first time in Italy. This species with a Paleotropi- cal geographical origin is a new invasive alien species in the flora of Italy. It was already reported in several European countries as invasive species, but this plant is also known for its medicinal properties in many areas of the world. The species was found in anthropic environments of Sicily. In particular, the study area is localized in the Peloritani Mounts (NE Sicily) where the species was discovered in five stands. Our new discovery confirmed the role that an- thropic activities have had in the spread of invasive alien species in Italy. Diagnostic features, ecological and geograph- ic data are provided. From a phytosociological viewpoint, this plant characterizes a plant community that includes various nitrophilous species such as Digitaria sanguinalis (L.) Scop., Eleusine indica (L.) Gaertn. and Sorghum halepense (L.) Pers. In addition, the invasiveness of and impacts associated with this species were assessed with the use of the EPPO prioritization protocol. The specimens were deposited in the herbaria of Catania and Messina University. Keywords: anthropogenic plant, biological invasion, neophyte, Sicily, vascular flora Introduction Urbanization and climate change encourage the inva- sion and spread of exotic plant species (Salinitro et al. 2019). In particular, several alien species have recently been report- ed 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 Bur- nett 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 com- plex due to its great changeability. Moreover, these species also usually grow in areas with a high degree of human in- trusion. 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, muti- cous to prominently aristate (Fryxell 1997). During field surveys in the northeast region of Sicily, we discovered several individuals of an unknown Sida repre- sentative mainly associated with urban areas. The plant was identified as Sida rhombifolia L. through literature and her- barium research. This species, widely distributed in the trop- ical, 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 prob- ably attributable to the Paleotropics (Verdcourt 2004). It is mainly known for its medicinal uses in tropical and subtrop- * Corresponding author e-mail: gianmarco.tavilla@phd.unict.it mailto:gianmarco.tavilla@phd.unict.it CAMBRIA S., CRISAFULLI A., DEL GALDO G. G., PICONE R. M., SOLDANO A., SCIANDRELLO S., TAVILLA G. 160 ACTA BOT. CROAT. 81 (2), 2022 ical areas worldwide (Ajeet et al. 2018), where it shows a po- tential 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 Sida spinosa L., which is reported as a ca- sual 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 re- ported 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 in- dicated 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 popula- tion of S. rhombifolia (the only population currently known in Italy). Additonally, the invasive behavior in and potential impacts on Italy have been assessed. Materials 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 sur- veys 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. Fig. 1. Drawing of Sida rhombifolia L. (Malvaceae) from living Sicilian specimens (by S. Casella): A ‒ flowering stem, B ‒ leaf abaxial surface, C ‒ leaf adaxial surface, D ‒ close-up of stellate hairs, E ‒ stipules, F ‒ flower, G1 ‒ schizocarp, G2 ‒ mericarps. SIDA RHOMBIFOLIA NEW ALIEN SPECIES FOR ITALY ACTA BOT. CROAT. 81 (2), 2022 161 (2017-2019), while the nomenclature was compiled follow- ing Bartolucci et al. (2018), Galasso et al. (2018) and subse- quent updates reported in the Portal to the Flora of Italy (2022). In addition, many herbarium sheets of S. spinosa and S. rhombifolia were carefully examined for the correct iden- tification 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 distri- bution 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), designat- ed 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; Napaea rhombifolia (L.) Moench, Metho- dus 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; Sida rhombifolia 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 campanu- late, 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, flat- tened 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). Fig. 2. Morphological features of leaves of Sida rhombifolia L. (Malvaceae): A ‒ leaf adaxial surface, B ‒ leaf abaxial surface, C ‒ detail of the leaf edge, D ‒ stellate hairs, E, F ‒ stipules. CAMBRIA S., CRISAFULLI A., DEL GALDO G. G., PICONE R. M., SOLDANO A., SCIANDRELLO S., TAVILLA G. 162 ACTA BOT. CROAT. 81 (2), 2022 Fig. 3. Fruit of Sida rhombifolia L. (Malvaceae): A ‒ frontal view of schizocarp B ‒ lateral view of schizocarp, C ‒ detaching mericarps, D ‒ frontal view of mericarp. Fig. 4. Distribution map of Sida rhombifolia L. (Malvaceae) in Peloritani in Sicily, Italy. to S. 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 Sida genus 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 fol- lowing 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 Sida rhombifolia was found in five localities of the Pelo- ritani 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 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 taxon- omy 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 SIDA RHOMBIFOLIA NEW ALIEN SPECIES FOR ITALY ACTA BOT. CROAT. 81 (2), 2022 163 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, Foeniculum vulgare Mill. Subsp. Vulgare, Rubus ulmifolius Schott, Geranium molle L., Malva sylvestris L., Oxalis pes-caprae L., Portulaca oleracea 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 commu- nities 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 Tab. 1. Phytosociological relevés of plant community with S. rhombifolia carried out in Messina province (NE Sicily, Italy). Place and date of relevés: Rels. 1-4: Rometta, 13. 11. 2020, Rels. 5-6: Valdina, 15 .4. 2021, Rels. 7-8: Furnari, 16. 4. 2021, Rel. 9: Terme Vigliatore, 16. 4. 2021, Rels. 10-12: Barcellona Pozzo di Gotto, 16. 4. 2021. Relevé number 1 2 3 4 5 6 7 8 9 10 11 12 Altitude (m a.s.l.) 10 10 10 10 18 18 17 17 65 14 14 14 Plot size (m2) 40 40 40 40 50 50 50 50 50 50 50 40 Vegetation cover (%) 80 80 90 90 80 80 90 90 80 90 80 90 Sida rhombifolia L. 3 2 2 2 3 2 2 1 2 3 4 3 Digitario sanguinalis‐Eragrostietea minoris Achyranthes sicula (L.) All. . . . . . . . . . + + + Amaranthus retroflexus L. . . . . . . . . . + + + Bidens pilosa L. . . . . . . . . 3 2 + 1 Boerhavia coccinea Mill. . . . . . . . . . . 1 1 Digitaria sanguinalis (L.) Scop. 2 + + . . 1 + + . + + . Eleusine indica (L.) Gaertn. . + + 1 . . + . . . . . Erigeron bonariensis L. . . . . . . 1 + . . + + Euphorbia prostrata Aiton . . . + + + . . + . . . Setaria verticillata (L.) P. Beauv. . . . + . . . . . . . . Sorghum halepense (L.) Pers. + + . + . . . . . . . . Symphyotrichum squamatum (Spreng.) G.L. Nesom 1 . . . 1 1 2 2 . . . . Rhamno-Prunetea Rubus ulmifolius Schott + 3 . . 1 2 . + + . . + Other species Arundo plinii Turra . . . . . . . 1 . . . . Bituminaria bituminosa (L.) C.H. Stirt. . . . . . . + + . + . . Convolvulus sepium L. . . 1 + . . . . . . . + Dittrichia viscosa (L.) Greuter subsp. viscosa . + . . 1 2 + + . . . . Equisetum arvense L. . . . + + . . . . . . . Foeniculum vulgare Mill. subsp. vulgare . + . . + . . . . . . . Galactites tomentosus Moench . . . . . . + . . . . + Geranium molle L. 1 . . . + . . . . + . . Hyparrhenia hirta (L.) Stapf subsp. hirta . . . . . . 1 + . . + + Lathyrus annuus L. . . . . . . + . . + . . Malva sylvestris L. . . . + . . . . . . . . Melilotus sp. + . + + . . . . . . . . Oxalis pes-caprae L. . . 3 3 . . + + + . . . Portulaca oleracea L. . + . . + . . . . . . . Reichardia picroides (L.) Roth . 1 . . . . . . . . . . Rhus coriaria L. . . . . . . . . + . . . Ricinus communis L. . . . . . . . . . . . + Rumex pulcher L. + . . . . . . . . . + + Sixalix atropurpurea (L.) Greuter & Burdet + . . . + + . . . . . . Sonchus tenerrimus L. . + . . + . . . . . . . Verbena officinalis L. . . + + + . . . . . . . Vicia sativa L. . . . . . . + + . . . . Vicia villosa Roth . + . . + + + . + + . . Xanthium strumarium L. . . . + . + . . . . . . CAMBRIA S., CRISAFULLI A., DEL GALDO G. G., PICONE R. M., SOLDANO A., SCIANDRELLO S., TAVILLA G. 164 ACTA BOT. CROAT. 81 (2), 2022 et al. 2010). In Sicily, it is locally well established and exhib- its high coverage with a growing number of individuals, ac- cording 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 al- most 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. Be- sides, the EPPO protocol (Branquart et al. 2016) was per- formed on S. rhombifolia. The result of the assessment (eval- uation of spread, impacts, and uncertainty degree) is shown in Tab. 2. Discussion This new record of S. rhombifolia for Italy seems to not show a high invasive potential of the species, despite its in- creasing spread in the Mediterranean Europe territories in recent years. This species in Sicily has not yet colonized hab- Fig. 5. Habit (A, B) of Sida rhombifolia L. (Malvaceae) (Sicily) with morphological details of the leaves (C), flower (D), and schizocarps (E). Tab. 2. Conclusions from the prioritization (stage 1: risk assessment): Sida rhombifolia L. was categorized in the European List of Mi- nor Concern (ELMC). Abbreviations: Aus ‒ Australia, Am ‒ America, Pal ‒ Paleotropical. Country abbreviations correspond to ISO codes. Under questions A8 and A9, uncertainty is represented by (L) low, (M) medium or (H) high. Species Sida rhombifolia L. A.1. Clear taxonomy Yes A.2. Alien in the EU Yes (Pal) A.3. Quality of information sufficient Low A.4. Established in the EU Yes (BE, CZ, ES, FR, GB, HR, NL, PT) A.5. Invasive outside the EU Yes (Aus, Am) A.6. Potential establishment in the EU Yes (DK, IT, LT, NO, SE, UA) A.7. Spread Medium A.8. Impact on native plant species Low (L): forms dense stands, not spread rapidly to the surrounding area A.9. Impact on ecosystem functions and services Low (L): until now, it spread only in urban areas Conclusion of stage 1 ELMC SIDA RHOMBIFOLIA NEW ALIEN SPECIES FOR ITALY ACTA BOT. CROAT. 81 (2), 2022 165 itats with a significant ecological value. However, in the fu- ture, based on its ecological requirements and ongoing cli- mate 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 known as “fiumare” (Habitat code 3290). Sida rhombifolia together with other invasive species reported from the Northeastern part of Sicily, such as Euphorbia hypericifolia L., Ailanthus altissima (Mill.) Swingle., Lantana camara 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 endem- ic 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 geo- graphical 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 spe- cies in the Sicilian territory, in order to supervise the expect- ed spread in the above mentioned habitats so as to limit al- teration of the floristic and structural composition of these environments. Specimina visa: Sida rhombifolia L.–Portugal: Azores, 1846, T. Hunt s.n. (BR0000013473679); India: Tamil Nadu Peninsula Indiae Orientalis Madras, 1867, Wight 166 (K000659356); Camer- oon: 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); Fairfield County, 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 Ca- selli 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 Incor- bina (Palermo), September 2001, S. Romano s.n. (PAL); Bra- zil: 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 Sebas- tião 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). Acknowledgements The authors wish to thank Salvatore Casella for having realized the drawing included in the text. We would also like to thank Giulia Giangravè, English native speaker, for the linguistic improvements to the manuscript. 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