The common chameleon Chamaeleo chamaeleon is a Mediterranean lizard which has been introduced in many islands and its native origin in European countries is debated. Chameleons have been introduced in southern Italy, possibly from the Middle East and Tunisia. We conducted genetic analyses on mitochondrial DNA 16S gene on a larger sample. We observed a multiple origin for the Salento (Apulia, southern Italy) population, with individuals phylogenetically related to populations of North Africa and two areas in the Middle East. Some individuals may have been released before the 1950s and some others in the 1980s, improving the establishment success of this species.

16S rRNA gene, Chamaeleo chamaeleon, Mediterranean countries, paleo-introduction, population origin

Genetics can play a crucial role in describing biological invasions, which are one of the major threats to global biodiversity (Vitousek et al. 1996; Schmitz and Simberloff 1997; Courchamp et al. 2017; Crooks et al. 2017). Accordingly, genetic variation can reveal taxonomic differences (Panzeri et al. 2014; Comtet et al. 2015; Mori et al. 2017; for a review, see Lawson Handley et al. 2011). A high genetic variability of the founders often results in a high colonization/invasion success (Mori et al. 2014; Jackson et al. 2015; Paulauskas et al. 2016). Genetics has been widely used to infer source populations and invasion paths (Stevenson-Holt and Sinclair 2015; Daane et al. 2018), which may help researchers to predict alien species’ spread and inform authorities how to prevent further invasions (Ciosi et al. 2010; Mazzamuto et al. 2016).

Chameleons (Squamata, Chamaeleonidae) include over 210 lizard species grouped in 12 genera (Tilbury 2018). Among those, the genus Chamaeleo is the only one naturally present in Mediterranean countries, North Africa and the Middle East (www.iucnredlist.org. Downloaded on 29 April 2018). Traditional taxonomy identified four subspecies of the common chameleon Chamaeleo chamaeleon (Yaacov et al. 2012; Andreone et al. 2016; Tilbury 2018), which live in allopatry in its natural range. As to Europe, populations in the Iberian Peninsula seem to have been introduced from Maghreb, with multiple introduction events (Paulo et al. 2002). Common chameleons currently present in Cyprus and in Greek islands (e.g. Samos, Chios and Crete) share mitochondrial haplotypes with the Turkish population (Macey et al. 2008; Andreone et al. 2016). At least two subspecies of the common chameleon have been introduced to Malta (Dimaki et al. 2008; Andreone et al. 2016), one from Maghreb and the other from the Near East. As for southern Italy, chameleons in Calabria (province of Reggio Calabria) were possibly introduced from Tunisia (Andreone et al. 2016). Conversely, Andreone et al. (2016) showed that the population of the common chameleon in Salento (Apulia) may originate from the Middle East, sharing mitochondrial sequences with Eastern Mediterranean countries (northern Israel). In southern Italy, long-lasting observational data and records of young individuals provide strong evidence of reproduction and naturalization (Marzano and Scarafino 2010; Pellegrino et al. 2016). Other observations from the rest of Italy (Sicily, Sardinia, Latium, Liguria, Emilia Romagna and Friuli Venezia-Giulia) refer to single individuals (Bruno 1986; Andreone et al. 2016) and, for most of them, no photos or tissue samples or museum specimens exist (Andreone et al. 2016).

Andreone et al. (2016) analyzed three individuals from Salento, collected in the same year (2015), from the same study site (i.e., Nardò). According to published works, the first record of the common chameleon in Salento in the wild dates back to 1987 and, since then, records have increased (Basso and Calasso 1991; Marzano and Scarafino 2010). Andreone et al. (2016) and Marzano and Scarafino (2010) confirmed that most records came from the municipality of Nardò. Given that both Costa (1871) and Bruno (1986) did not report the presence of the chameleon in Salento, Andreone et al. (2016) claimed that the presence of the chameleon in this area might be the result of a recent introduction (e.g. early 1980s: see Scalera 2001). Conversely, Basso and Calasso (1991) already reported that the distribution of this small lizard could be even wider and possibly date back prior to 1980. In this work, we aimed at (i) mapping the local distribution of the common chameleon in Salento which underwent a range expansion, (ii) to identify the subspecies and (iii) to infer the origin of common chameleon established in this area.

Despite the high number of single records of this species throughout Italy in the wild (Andreone et al. 2016), only two established populations of the common chameleon seem to currently occur in southern regions, i.e. in Calabria and in Apulia (Basso and Calasso 1991; Pellegrino et al. 2016). The first is located in the province of Reggio Calabria, in the surroundings of Palmi (Pellegrino et al. 2016), whereas the second one has been only reported to occur in the surroundings of Nardò (province of Lecce, Salento, Apulia: Scalera 2001; Andreone et al. 2016). Our work showed that the distribution of the common chameleon in Salento is wider than previously known (i.e. potentially only the municipality of Nardò: Scalera 2001; Andreone et al. 2016), encompassing a 515 km² area on the Ionian coast between the municipalities of Nardò and Castrignano del Capo. The species is well-established and possibly expanding in this area, as confirmed by reports of reproductive females, eggs and juvenile individuals. Our genetic analyses also showed that chameleons currently present in Salento may belong to at least three subspecies. Andreone et al. (2016) reported that this lizard was introduced from Lebanon at the end of the 1980s; in our work, we showed that multiple introductions likely took place even before the 1980s, leading to the current lineage mix. According to our results, the common chameleon may represent an historical introduction in Salento, as already reported for the Iberian Peninsula (southern Spain and Portugal: Paulo et al. 2002) and Malta (Dimaki et al. 2008). Andreone et al. (2016) amplified very recent samples of common chameleon from Salento, which fell within the “recticrista” clade, together with Turkish, Samian, Cypriot and northern Israeli sequences.

The species originated in the Arab peninsula, with the subspecies C. c. orientalis being the oldest one, and evolved in Maghreb and southern Middle East; the most recent subspecies seems to be C. c. recticrista (Andreone et al. 2016). As to our samples, all the oldest samples belonged to Middle-Eastern mitochondrial clades (namely, “recticrista” and “musae”: Yaacov et al. 2012), whereas a high number of the most recent ones belonged to the North African (“chameleon”) clade. This confirmed our hypothesis of multiple releases in the study area.

Worldwide, apart from the common chameleon, alien chameleon populations are only represented by escapes of pet-chameleons (i.e. the veiled chameleon and the Oustalet’s chameleon Furcifer oustaleti in Florida and the Jackson’s chameleon Trioceros jacksonii in Hawaii: Krysko et al. 2004; Holland et al. 2010; Kraus et al. 2012; Smith et al. 2016). The veiled chameleon has been released to Florida since 2000 with a high propagule pressure (i.e. over 100 founders), but, despite its range is growing (Gillette and Krysko 2012), ecological impacts on native environments have not been studied yet (Krysko et al. 2004). The introduction of the Jackson’s chameleon to Hawaii dates back to the 1970s, where it might have affected native endangered invertebrates (e.g. Achatinella mustelina: Chiaverano and Holland 2014) and, in turn, breeding warblers and honeycreepers (Scalera 2001; Holland et al. 2010; Kraus et al. 2012). The establishment of the Oustalet’s chameleon in the Everglades (South Florida) has been only recently assessed (Gillette et al. 2010; Smith et al. 2016) and data on the impact on native environments are not available. In the Hawaii archipelago, the veiled chameleon was eradicated in 2008, and a control program on the Jackson’s chameleon is currently ongoing (Van Kleeck and Holland 2017).

Management of alien species, including alien chameleons, is pivotal for conservation, and eradication or numerical control are strictly required to prevent environmental alterations (Menchetti and Mori 2014; Pergl et al. 2016; Crowley et al. 2019). Alien species taxonomy and local ecology are paramount to build effective and reliable models to predict their range expansion and impacts (Sitzia et al. 2016; Buchadas et al. 2017; Davis et al. 2019; Mori et al. 2019). The ecology of the common chameleon in European countries, including its potential impacts on native species, is still not well known and, thus, it deserves further research in order to design addressed management plans.

Climatic matches and repeated introduction events may have favored the establishment success of the common chameleon in southernmost parts of Spain, Portugal, Greece and Italy, whereas introductions failed elsewhere (central Italy, northern Spain: Scalera 2001).

In Europe, although representing a historically introduced species, the common chameleon is strictly protected as it has long been considered a native taxon in all Mediterranean countries (Paulo et al. 2002). This species is listed within the Appendix II of the Bern Convention and within the Annex IV of the Habitat Directive (92/43/EEC), requiring a strict protection regime throughout its European extent of occurrence, in areas where it is believed to be native, e.g. Iberian peninsula, but not Italy, where it is claimed to be alien (Genovesi et al. 2014). Our results confirmed that introductions of this species in Italy have occurred before the 1980s. After pertinent ecological studies, management interventions may become necessary, in accordance with European guidelines (Genovesi et al. 2014; Pergl et al. 2016; Shackleton et al. 2019).

Prof. Ilaria Corsi (University of Siena) kindly made available the facilities for genetic analyses, which were directly financed by the Museo Civico di Storia Naturale di Jesolo.

Data on the distribution and samples of the common chameleon in Salento were collected through the priceless help of Angelo Sodo † (Praetor of Nardò), Prof. Pietro Parenzan † (Director of the Marine Biology Station of Porto Cesareo and Museo del Sottosuolo di Taranto), Dr. Cosima Maglie † (pharmacist of Lecce), Dr. Raffaele Congedo † (Corpo Forestale dello Stato, Lecce) and Dr. Sandro D’Alessandro (Corpo Forestale dello Stato). We also thank the active members of the Salento Association A.R.C.A. 113 Ecologico Onlus. We acknowledge Bernardo Borri, Rudy Zozzoli and Francesco Ferretti for their help in analysis preparation. Dr. Vasco Sfondrini kindly took the time to revise the English grammar and syntax of our manuscript. The authors declare that they have no conflict of interest. The authors also confirm that, with regard to their manuscript, the guidelines for “Good Scientific Practice”, and concerning the studied animals, the applicable national and international regulations, were observed. All co-authors know about the submitted paper and agree with its submission in the present form. Maria Dimaki, two anonymous reviewers and the editor Günter Gollmann kindly provided us with useful comments on an early draft.

RB, MS and EM conceived the idea. RB and MS collected the samples. MLV and EM carried out the genetic analyses and LN did the phylogenetic reconstructions. EM and GM wrote most of the paper. All authors participated in writing the final manuscript.