Trade and Stowaways: Molecular Evidence for Human-Mediated Translocation of Eastern Skinks Into the Western Mediterranean

Home , Chalcides bedriagai, Chalcides ocellatus

Amphibia-Reptilia (2019) DOI:10.1163/15685381-20191249 brill.com/amre

Trade and stowaways: molecular evidence for human-mediated translocation of eastern skinks into the western Mediterranean

Josep Francesc Bisbal-Chinesta1,2,8,∗,KarinTamar3, Ángel Gálvez4,8, Luís Albero5,8, Pablo Vicent-Castelló6,8, Laura Martín-Burgos7, Miguel Alonso8, Rubén Sánchez8,CarlosOrtega8, Antonio Gómez8, David Candel8, Miguel Cervera8, Salvador Carranza3, Hugues-Alexandre Blain1,2

Abstract. Human movements in the regions surrounding the Mediterranean Sea have caused a great impact in the composition of terrestrial fauna due to the introductions of several allochthonous species, intentionally or not. Reptiles are one of the groups where this anthropic impact is most evident, owing to the extensive intra-Mediterranean dispersals of recent chronologies. Chalcides ocellatus is a widespread skink with a natural distribution that covers almost the entire Mediterranean Basin. Two hypotheses have been proposed to explain its origin: natural dispersions and human translocations. Previous molecular data suggest the occurrence of a recent dispersal phenomenon across the Mediterranean Sea. In this study we present the ﬁrst record of this species in the Iberian Peninsula, in Serra del Molar (South-east Spain). We combined molecular analyses and archaeological records to study the origin of this population. The molecular results indicate that the population is phylogenetically closely related to specimens from north-eastern Egypt and southern Red Sea. We suggest that the species arrived at the Iberian Peninsula most likely through human-mediated dispersal by using the trade routes. Between the Iron to Middle Ages, even now, the region surrounding Serra del Molar has been the destination of human groups and commercial goods of Egyptian origins, in which Chalcides ocellatus could have arrived as stowaways. The regional geomorphological evolution would have restricted its expansion out of Serra del Molar. These ﬁndings provide new data about the impact of human movements on faunal introductions and present new information relating to mechanisms of long- distance translocations.

Keywords: Chalcides ocellatus, DNA, introduction, Mediterranean Sea, reptiles, Spain, species dispersal.

Introduction

1 - Unitat de Paleontologia, Institut Català de Paleoecologia The Mediterranean Basin has been and still is Humana i Evolució Social (IPHES), Ediﬁci W3, Zona Educacional 4, Campus Sescelades, Universitat Rovira i a fascinating biogeographical framework pre- Virgili, 43007 Tarragona, Spain senting constant faunal exchanges, which have 2 - Àrea de Prehistòria, Departament d’Història i Història affected many of the faunas present on every de l’Art, Facultat de Lletres, Universitat Rovira i Vir- gili (URV), Avinguda de Catalunya 35, 43002 Tarrag- shore of the Mediterranean and which have ona, Spain been augmented by human intervention (Poo- 3 - Institute of Evolutionary Biology (IBE-CSIC/Universi- ley and Queiroz, 2018). The distribution and in- tat Pompeu Fabra), Passeig Marítim de la Barceloneta, 37-49, 08003 Barcelona, Spain ferred phylogeographic patterns of reptiles such 4 - Institut Cavanilles de Biodiversitat i Biologia Evolutiva as the circum-Mediterranean geckos Tarentola (ICBiBE), Universitat de València. C/ Catedràtic José mauritanica and Hemidactylus turcicus have Beltrán Martínez 2, 46980 Paterna, València, Spain 5 - Área de Ecología, Departamento de Biodiversidad y suggested the existence of possible human in- Gestión Ambiental, Facultad de Ciencias Biológicas, terventions in their intra-Mediterranean disper- Universidad de León (ULE). Callejón Campus Veg- azana s/n, 24071 León, Spain sals (Harris et al., 2004; Carranza and Arnold, 6 - Museo Nacional de Ciencias Naturales (MNCN-CSIC), 2006; Rato et al., 2011, 2016; Stöck et al., C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain 2016). This phenomenon has also affected the 7 - EMCUJU Archaeologist, Ayuntamiento de Alpuente, C/ Rey Don Jaime 5, 46178 Alpuente, València, Spain Iberian Peninsula, which shares many species, 8 - Secció de Estudis Cientíﬁcs, Associació Herpetològica Timon (AHT), C/ València 32, 46195 Llombai, Valèn- cia, Spain ∗Corresponding author; e-mail: [email protected]

© Koninklijke Brill NV, Leiden, 2019. DOI:10.1163/15685381-20191249 2 J.F. Bisbal-Chinesta et al. both reptiles and amphibians, with North Africa the eastern Moroccan coast to Anatolia, as well (Pleguezuelos et al., 2008). Human transloca- as on various islands in the Aegean Sea, Eu- tions with North African origin are proposed boea, Crete, Cyprus, Tunisian Tabarka, Malta, for the Iberian populations of the chameleon Sicily, Conigli, Lampedusa, Lampione, Linosa Chamaeleo chamaeleon (Paulo et al., 2002) and and Sardinia, with continental European popu- the treefrog Hyla meridionalis (Recuero et al., 2007). Other dispersals, on the other hand, have lations in and into the Attica peninsula (Kornil- their origins in the Iberian Peninsula, for ex- ios et al., 2010). The species’ distribution range ample, the translocation of the lizard Podar- also extends to the Near East, Mesopotamia, and cis vaucheri in Greece (Spilani et al., 2018). In the shores of the Red Sea, as far south as So- the Western Mediterranean context, the human- malia and Yemen, and in the Persian Sea re- mediated introductions of herpetofauna in the gion as far east as Pakistan (Anderson, 1999; Balearic Islands stand out, where the successive arrivals of different human groups led to Lavin and Papenfuss, 2012). There are cur- the extirpation of native species in most of the rently introduced populations in Naples, Strom- main islands (Alytes muletensis and Podarcis lil- boli, Kasos and Sri Lanka (Caputo et al., 1997; fordi), besides the introduction of new species Karunarathna et al., 2009; Lo Cascio and Grita, from other Mediterranean regions (e.g. Bu- 2016; Kornilios and Thanou, 2016), as well as in fotes balearicus, Emys orbicularis, Testudo her- Florida and Arizona (Krysko et al., 2011; Gunn manni, Podarcis sicula, and Hemorrhois hip- et al., 2012). Three Algerian individuals were pocrepis), from the Neolithic-Bronze Ages to the present (Pinya and Carretero, 2011; Valen- released in Marseille (France) and created a new zuela et al., 2016; Silva-Rocha et al., 2018). population during the ﬁrst decades of the 20th Another reptile species with a practically century, and an isolated individual was found in circum-Mediterranean distribution is the ocel- the railway goods yards of Cardiff (Wales) in lated skink, Chalcides ocellatus, which can 1944 (Siépi, 1913; Fitter, 1959; Kraus, 2009). be considered a species complex, with sev- The large transcontinental distribution of C. eral deep lineages across North Africa (Car- ranza et al., 2008). This skink is widely dis- ocellatus, together with the low molecular di- tributed in the southern, central and eastern re- vergence and the hard polytomies observed gions of the Mediterranean basin (ﬁg. 1), from among many of the populations assigned to the

Figure 1. Mediterranean distribution range of Chalcides ocellatus according to its phylogenetic clades (Kornilios et al., 2010) and the geographic location of the Serra del Molar population (SE Iberian Peninsula; blue star). Arrows indicate the Phoenician intra-Mediterranean maritime routes and the main trade ports during the first Iron Age period (black dots) (based on Aubet, 2009). Human translocation of skinks across the Mediterranean Sea 3 eastern subclades, have made it possible to pos- Peninsula, molecular analyses were performed tulate the human-mediated introduction in re- to confirm its identification and to determine the cent times as a possible mechanism for its ex- biogeographical origin of this newly discovered pansion (Kornilios et al., 2010; Lavin and Pa- population. penfuss, 2012), and even link it, at least in the context of the Mediterranean Sea, to the trade during the Ancient Age (Kornilios et al., 2010). Material and methods In this study, we report for the first time Individuals of C. ocellatus were identified for the first time the presence of a reproductive population of in April 2017 in Serra del Molar (38.1439N, −0.6569W, C. ocellatus WGS; fig. 1). This area is part of the Elx municipality, in the ocellated skink, , in Serra del the Baix Vinalopó comarca within the Valencian province Molar (fig. 2). The geographic location of the of Alacant/Alicante, in the grid UTM 30SYH02. The area population is a small coastal mountainous area where the discovery took place is between 35 and 75 me- ters above sea level, presents a Mediterranean thermos-type in the southeast of the Iberian Peninsula, lo- and is biogeographically located in the Alicantino subsector calised between the Mediterranean Sea and of the Murciano-Almeriense sector (Rivas-Martínez, 1987). marsh areas originated by the Vinalopó and Se- It is a predominantly sedimentary area, formed at its base by calcareous sandstones of coastal marine origin on which gura rivers, in the southern Valencian Country. outcrop conglomerates of silt, marl and fluvio-lacustrine These individuals were morphologically identi- sands (Almela et al., 1978). The area presents the typical fied as C. ocellatus (body elongate and cylindri- thermo-Mediterranean scrub communities (Brachypodium retusum, Macrochloa tenacissima, Rosmarinus officinalis, cal, tail almost equal to body length, ear with- Chamaerops humilis) with concentrations of Pinus halepen- out lobules, tympanum exposed, multiple dor- sis, and only the lower parts show evidence of abandoned sal ocelli; Baha El Din, 2006). Given that this plots for cultivation of olives (Olea europaea) and carobs (Ceratonia siliqua), although today most of them are cover- is a species without current herpetological or ed by xerophilous and heliophilous scrubs. The archaeolog- archaeo-paleontological records in the Iberian ical remains of the Iberian settlements of La Escuera and El

Figure 2. Individuals of Chalcides ocellatus from Serra del Molar (SE Iberian Peninsula): (A) Adult male (♂ n.3, CN12645); (B) Adult male (♂ n.4); (C) Gravid female (♀ n.2); (D) Adult male in its habitat (♂ n.5, CN13391). 4 J.F. Bisbal-Chinesta et al.

Table 1. Morphometric data of the Chalcides ocellatus individuals from Serra del Molar. Specimens used for the genetic identiﬁcation are with their corresponding code. (*) = autotomized and partially regenerated tails.

Individuals Body length Tail length Total length Tail/body ratio (SVL; in mm) (in mm) (in mm)

Male n.1 95.2 100.5 195.7 1.05 (01.04.2017) Male n.2 85.891.9 177.7 1.07 (01.04.2017) Male n.3, CN12645 99.1 101.7 200.8 1.02 (07.10.2017) Male n.4 (20.04.2018) 102.176.8∗ 178.9 0.75 Male n.5, CN13391 97.273.2∗ 170.4 0.75 (18.05.2018)

Female n.1 96.092.4 188.4 0.96 (02.04.2017) Female n.2, gravid 105.1 115.4 220.5 1.09 (11.06.2017) Female n.3, gravid 89.490.7 180.1 1.01 (11.06.2017) Female n.4, CN12564 84.386.6 170.9 1.03 (08.10.2017) Female n.5 (20.04.2018) 84.335.4∗ 119.7 0.42 Female n.6, CN13435 78.489.3 167.7 1.14 (18.05.2018) Female n.7, CN13434 76.883.5 160.3 1.08 (18.05.2018)

Median ± Standard error (SE) 91.14 ± 2.738 86.45 ± 5.658 177.59 ± 7.115 0.95 ± 0.142 Median ± Standard error (SE) 90.01 ± 3.265 94.67 ± 3.259 184.68 ± 6.252 1.05 ± 0.111 (without autotomized tails)

Oral, and the necropolis of El Molar are located in the sur- the Mediterranean Basin and across the species’ distribu- roundings (Grau and Moratalla, 2001). According to data tion range, were retrieved from GenBank. Two specimens of from official herpetological agencies (AHE, 2018; BDB- Chalcides montanus have been included as outgroup (Car- GVA, 2018), the reptiles of this area had not been surveyed ranza et al., 2008; Kornilios et al., 2010) (see supplementary previously by any herpetologist or scientific group. table S1 and supplementary fig. S1). In collaboration with the Valencian environmental au- Genomic DNA was extracted from alcohol-preserved tis- thorities, successive surveys were carried out in this local- sue samples using the SpeedTools Tissue DNA Extraction ity to monitor their presence in the area, to obtain data on kit (Biotools, Madrid). A fragment of 303 bp of the mito- their spatial distribution and morphology, and to obtain tis- chondrial gene Cytochrome b (cytb) was amplified by the sue samples for genetic analyses. Twelve identified individ- Polymerase Chain Reaction (PCR). The following primers uals were captured to obtain morphometric data and subse- for amplification and sequencing were modified from quently released (table 1). Each individual has been sexed Kocher et al. (1989): Cytb1 (5-CCATCCAACATCTCAGC by pressing gently around the cloacal region to find the ATGATGAAA-3)andCytb2(5-CCCTCAGAATGATATT hemipenises, if males. Importantly, this process was con- TGTCCTCA-3). We performed PCR in a volume of 25 μl ducted avoiding the total eversion of hemipenises to avoid with an initial denaturation step of 94°C for 5 min, followed potential injuries for the animals. by 35 cycles of denaturation at 94°C for 80 s, annealing at 50°C for 45 s, and extension at 72°C for 1 min; final exten- Genetic sampling, DNA extraction and amplification sion step was set for 72°C for 5 min. Amplicons were visualized on a 1% agarose gel stained with SYBR Safe DNA gel In order to perform molecular analyses, tissue samples stain (Invitrogen Corp., Carlsbad, CA, USA). Purification were taken from five individuals with the following sample and bi-directional sequencing were carried out by Macrogen codes: CN12564 and CN12645 were collected during Octo- (Macrogen Inc.). Chromatographs were checked and the ber 2017, and CN13391, CN13434 and CN13435 were col- forward and reverse sequence contigs for each sample were lected in May 2018. To understand the geographic origin of assembled and edited using Geneious v.7.1.9 (Biomatter these newly discovered Valencian individuals, sequences of Ltd.). Sequences were aligned using MAFFT v.7.3 (Katoh other C. ocellatus specimens from distinct localities around and Standley, 2013) with default parameters. We translated Human translocation of skinks across the Mediterranean Sea 5 the final alignment into amino acids and no stop codons with exposed tympanum; biometric tail/body ra- were detected. tio (tail length divided by distance from snout tip to cloaca) very close to value 1 (average: Phylogenetic analyses 1.05, range: 1.14–0.96; table 1); pentadactyl Phylogenetic analyses were performed under maximum front limbs with phalangeal formula 2.3.4.4.3; likelihood (ML) and Bayesian inference (BI) frameworks. and pentadactyl hind limbs with phalangeal for- The ML analysis was conducted in RAxML v.8.1.2 as implemented in raxmlGUI v.1.5 (Silvestro and Michalak, mula 2.3.4.5.3. The animals present the typical 2012). The analysis was performed with the GTR+G model body-form and colouration pattern of the sub- of sequence evolution and 100 random addition replicates. species C.ocellatus ocellatus (fig. 2). Nodal support was assessed with 1000 bootstrap replicates. The BI analysis was conducted with BEAST v.1.8.4 (Drum- mond et al., 2012). We used jModelTest v.2.1.7 (Guindon and Gascuel, 2003; Darriba et al., 2012) to select the best Phylogenetic structure model of nucleotide substitution under the Bayesian information criterion (BIC). We carried out the BEAST analy- The dataset of the cytb gene used in the phylo- sis with the following priors (otherwise by default): TrN+G genetic analyses included 153 sequences of C. model; Coalescent: Constant size tree model; random start- ocellatus and had a total length of 303 bp: five ing tree; alpha prior uniform (0–10); uncorrelated relaxed clock (uniform distribution; 0–1). Three individual runs of newly discovered individuals from Spain, 146 2 × 106 generations were carried out, with sampling at in- sequences from across the Mediterranean Sea tervals of 2 × 103 generations. Convergence, posterior trace and adjacent regions, and two specimens of C. > plots, effective sample sizes ( 200), and burn-in were eval- montanus (see supplementary table S1 and fig. uated with Tracer v.1.6 (Rambaut et al., 2014). The tree runs were combined in LogCombiner discarding the first 10% S1). The ML and BI phylogenetic trees present of the trees as burn-in and the ultrametric tree was gen- a structure of three clades within C. ocellatus erated with TreeAnnotator (both available in the BEAST (fig. 3, supplementary fig. S1) separated into the package). Phylogenetic trees were visualized with FigTree v.1.4.3 (Rambaut and Drummond, 2010). eastern, central and western coastal areas of the Mediterranean Sea. Within these clades, a geographic grouping of specimens is apparent, al- Results though with an unsupported topology. In both the ML and BI analyses, Serra del Molar in- Between April 2017 and May 2018, 35 individ- dividuals are nested within a clade with speci- uals of C. ocellatus were identified, from which mens from the eastern Mediterranean region. morphometric measurements of 12 distinct in- Four of the five Spanish specimens dividuals could be obtained, all were adults (CN12645, CN13391, CN13434 and CN13435) (snout-vent length, SVL > 55 mm, Çiçek et al., cluster together with two Egyptian individu- 2013) (table 1). The different attested stages of als with high support (bootstrap and poste- ontogenetic development have allowed verify- rior probability values, 96 and 1, respectively). ing the existence of a breeding population, with These Egyptian specimens (co50-FJ980237 and young and adult individuals, besides the pres- co51-FJ980238; Kornilios et al., 2010) were ence of gravid females (fig. 2c). The popula- collected from Ras El Barr, in the Damietta tion is distributed at least in a spatial range of Branch of the eastern Nile Delta. The sequences 5.2 km2. of these six specimens (Serra del Molar-Spain The preliminary taxonomic assignment of and Ras El Barr-Egypt) are almost identi- Serra del Molar individuals into C. ocellatus cal, apart from one single mutation in posi- has been confirmed, following the criteria of tion 159 where the Spanish specimens have Baha El Din (2006) and Carranza et al. (2008): an A, whereas the Egyptian specimens have primitive corporal form within the Chalcides a G. The fifth Spanish individual (CN12564) genus, elongate and cylindrical; black and white has a different phylogenetic position, cluster- dorsal ocelli; atrial overture markedly visible, ing with samples from Egypt (including four 6 J.F. Bisbal-Chinesta et al.

Figure 3. Bayesian Inference Cytochrome b phylogenetic tree of Chalcides ocellatus. Bootstrap (ML) and Bayesian posterior probabilities (BI) support values are indicated above and below the nodes, respectively. The newly discovered Spanish specimens collected from Serra del Molar are highlighted. Sample codes and localities correlate to specimens in supplementary table S1. Human translocation of skinks across the Mediterranean Sea 7

Egyptian specimens that were collected from fig. S1), which has been identified in other Ras El Barr, co48-FJ980235, co49-FJ980236, human-mediated lizard introductions (Kolbe et co52-FJ980239 and co53-FJ980240), Soma- al., 2007; Santos et al., 2019), suggests the con- lia, Libya, Yemen, Turkey, Syria, Greece, and currence of at least two translocation events Cyprus, although with no support. This speci- with distinct sources that originated the new men’s sequence is different from the other Span- population, or a single introduction with in- ish individuals in seven positions (in sites: 60, G dividuals from multiples origins, or that the vs. A; 96, A vs. C; 105, T vs. C; 129, C vs. G; admixture was already present at the original 144, T vs. C; 204, G vs. A; 285, C vs. T, respec- population or locality, as happens in Ras El tively). Barr. The dispersal mechanism linked to human ac- tivities has been one of the explanations given Discussion to the wide distribution of C. ocellatus (Schnei- Two hypotheses have been proposed to explain der, 1981; Anderson, 1999) and is consistent the origin of the Mediterranean populations of with the phylogenetic studies (Carranza et al., C. ocellatus: natural dispersal (maritime, conti- 2008, Kornilios et al., 2010; Lavin and Papen- nental or through temporary terrestrial bridges) fuss, 2012). In fact, there is a historical record and human translocations (Lavin and Papen- of its introduction into Naples in a shipment fuss, 2012). The molecular results rule out any of orange trees from Sicily during the 18th scenario of natural colonization of C. ocellatus century AD (Caputo et al., 1997). Other au- in Serra del Molar: the phylogenetic tree as- thors propose different translocation methods, signed Serra del Molar individuals within sub- like the use of sand ballasts and their subsequent clade A2, distributed across the eastern Mediter- abandonment in port areas of the Persian Sea ranean basin (Kornilios et al., 2010) and ex- (Anderson, 1999). The widespread distribution clude their arrival by “rafting” or other natu- of the subclade A2 in Kornilios et al. (2010) ral dispersal by sea from the Tunisian, Algerian has been associated with maritime exportation or Moroccan coasts, which are the nearest nat- routes of the Silphium plant during the Ancient ural populations of ocellated skinks (Martín et Age (7th-2nd centuries BC), a trade originating al., 2017; Beddek et al., 2018). Additionally, the in Libyan-Hellenic Cyrenaica (Amigues, 2004), populations of C. ocellatus from these Maghre- as one of the ways by which C. ocellatus ex- bian countries belong to other phylogenetic panded through the Eastern Mediterranean (Ko- clades (Carranza et al., 2008; Kornilios et al., rnilios et al., 2010). 2010; fig. 3, supplementary fig. S1). Moreover, The regional archaeological record of Serra the extremely low genetic divergence found in the molecular data and the phylogenetic posi- del Molar has many peculiarities that allow us to tion of the Serra del Molar individuals allow to postulate the possibility of an introduction due rule out their spread by land through a conti- to intra-Mediterranean maritime trade. The sur- nental bridge within a very old paleogeographic rounding region presents an important archae- scenario (for example, during the Messinian ological record linked to trade with the East- Salinity Crisis). Therefore, the genetic assigna- ern Mediterranean and Phoenician colonization tion in the eastern Mediterranean subclade im- during the second quarter of the 1st millen- plies that the only reasonable and plausible sce- nium BC, associated with the Phoenician colony nario is the human-mediated translocation. of La Fonteta (Guardamar del Segura), which The presence of a genetic admixture among is located 2.5 kilometres from Serra del Mo- the ocellated skinks from Serra del Molar lar (González, 2010a, b; Doménech, 2010) (fig. (supplementary table S1 and supplementary 4b). 8 J.F. Bisbal-Chinesta et al. Human translocation of skinks across the Mediterranean Sea 9

The five sequenced individuals from Serra del themselves (Buxó, 2008; Iriarte et al., 2016). Molar belong to the same subclade A2 in Ko- The molecular data of the conifer Tetraclinis rnilios et al. (2010) and appear to be mainly articulata from the nearby Sierra de Cartagena linked with the Egyptian specimens sampled (Murcia), which suggest the introduction or lo- from Ras El Barr, in the Nile Delta. During cal genetic substitution through translocations the ancient past, in this same area of Lower from Tunisia by the Phoenicians/Carthaginians Egypt were seaports that traded with other (Sánchez-Gómez et al., 2013), show the human- regions across the Mediterranean Sea, such mediated mobility of plant species across the as Naukratis, Thonis-Heracleion, Tamiat, Pelu- Mediterranean Sea during this same chronol- sium and Tell el-Ghaba (Stanley et al., 2008; ogy. Pfeiffer, 2010; Lupo and Kohen, 2010), all of In the context of ancient Mediterranean in- them were active harbours during the same pe- teractions, similar mechanisms of translocation riod as La Fonteta colony (8th–6th centuries have been proposed for the colonization of BC). In this Phoenician settlement and in nearby Vipera aspis hugyi on the island of Montecristo contemporary sites, a large amount of Egyptian (Masseti and Zuffi, 2011) and the introduction objects has been discovered together with other of Eryx jaculus in the Licata region, Sicily (In- manufactures from eastern workshops (Padró, sacco et al., 2015). The presence of ocellated 1975; Doménech, 2010; Escolano, 2012; López skinks in this Iberian region, archaeologically and Velázquez, 2012; González, 2014; Martínez linked to the Eastern Mediterranean, reinforces and Vilaplana, 2014). the hypothesis of Kornilios et al. (2010) about A possible route for the ocellated skink the ancient trade as the main phenomenon for translocation is its arrival as an unintentional the dispersal of C. ocellatus, and reinforces cargo passenger along with merchandises from Egypt as the possible main point of the human- Egypt (or another nearby eastern Mediterranean mediated translocations. region) to the Phoenician colony of La Fonteta However, the links between the Iberian south- and its later establishment in the periphery of east with the Eastern Mediterranean, and espe- one of its associated Iberian settlements lo- cially with Egypt, are not limited to the phe- cated in Serra del Molar, which was part of nomena of Iron Age trade and Phoenician colo- its most direct area of influence. The skinks nization, because the intra-Mediterranean con- could have arrived inside imported plants or tacts continued during the Roman dominion. soils, as is proposed by Kornilios et al. (2010) as More recent historical relations with Egypt oc- way for human-mediated dispersals of C. ocel- curred during early Middle Age, when Islamic latus in the eastern Mediterranean regions, in Egyptian troops colonized the surrounding re- which the skinks were transported as involun- gion of Tudmîr in 743 AD (Gutiérrez, 1996; tary stowaways. For example, another agricul- Vallvé, 1999). The Middle Age manuscripts tural product that could be the transport means also relay the existence of direct trade be- for the translocation were eastern varieties of tween Tudmîr and the harbours of the Fatimite vine strains (Vitis vinifera), during the introduc- Caliphate and Ayyubid Sultanate, particularly tion of viticulture in Iberia by the Phoenicians the Egyptian port of Alexandria (Azuar, 2016).

Figure 4. Biogeographical scenario for a Phoenician translocation of Chalcides ocellatus into the south-eastern Iberian Peninsula. (A) Serra del Molar as an island, isolated from the mainland by the Mediterranean Sea, during most of the Holocene. (B) Reconstruction of the area during the 8th-6th centuries BC, the formation of a coastal lagoon environment, the position of La Fonteta Phoenician colony and the main ﬁndings of objects with Egyptian origin (red point) in the southern Valencian Country. (C) Current situation of Serra del Molar and the current locality of the Chalcides ocellatus population (star). *Paleoenvironmental reconstruction of Serra del Molar during the Holocene to the present is based on Blázquez (2001), Grau and Moratalla (2001), Blázquez and Usera (2010), and Tent-Manclús (2012). 10 J.F. Bisbal-Chinesta et al.

One of the most important contributions that brackish marsh conditions until the 18th cen- the Muslim period had in the southern Valen- tury AD (Blázquez, 2001; Grau and Moratalla, cian area was the introduction of the “oasis 2001; Blázquez and Usera, 2010; Tent-Manclús, crop”. Its greatest exponent is the “Hort de 2012) (fig. 4b). Palmeres d’Elx” (Palm Grove of Elche), a large The preservation of quasi insular conditions monoculture concentration of the date palm until relatively recent times (fig. 4c) could have (Phoenix dactylifera) originated in the 10th cen- enabled the survival of C. ocellatus, in case tury AD that continues at present (Azuar, 1998). of an ancient introduction. To date, we were During the last decades, palm trees have addi- only able to locate individuals of ocellated skink tionally been used as ornament in private garin the north-east quadrant of Serra del Mo- dens and public parks. This requirement for new lar, which comparatively has suffered less an- trees, which could not be serviced only by local thropic impact, although this range may be production, was supplied by importing plants much larger due to the fossorial cryptic nature from Argentina and Egypt (Berbegal, 2017). of this skink. Most of the area preserve the typ- Due to the growing demand, the invasive red ical autochthonous scrubs with Aleppo pines palm weevil (Rhynchophorus ferrugineus)was and only the lowlands show evidences of old introduced in Spain mainland through the entry plots, though nowadays are abandoned. Today, of Egyptian palms without phytosanitary con- the biggest anthropic impact is the massive ur- trol in 1995 (Ferry and Gómez, 2002). The im- banization, such as estates and roads, in the portation of Egyptian palm trees or another an- southern half of Serra del Molar. New faunal thropogenic factors (including the current pet surveys will help to clarify and more accurately trade) may also explain a more recent origin for assess the distribution of C. ocellatus, since it is the translocation and colonization of Serra del a generalist species, cryptic and adaptable to the Molar. In addition, C. ocellatus have demon- presence of humans and agriculture (Schneider, strated a high capacity to colonize new areas 1981; Schleich et al., 1996). due to passive dispersals, recently documented An alien population of C. ocellatus in the in the islands of Stromboli (Italy) and Kasos Iberian Peninsula raises a new management (Greece) or even in America mainland (Florida problem: the possibility of an ancient introduc- and Arizona), where the ocellated skink was ab- tion in Serra del Molar, in addition to the semi- sent in thorough herpetological surveys a few insular character of this area, could be argu- years ago (Krysko et al., 2011; Gunn et al., ments for its conservation. On the other hand, 2012; Lo Cascio and Grita, 2016; Kornilios and the possible competition with the native skink Thanou, 2016). Chalcides bedriagai and the current connec- Regardless of the possibility of an introduc- tivity with the surrounding regions, may raise tion during Phoenician times, Islamic period or arguments to control its population and even more recently, the evolution of the Serra del propose its eradication. Following the guide- Molar’s environment could explain the survival lines of the recent review about the status of of an allochthonous population. Although cur- allochthonous herpetofauna in Spain and man- rently it is connected to the continent (fig. 4c), agement proposals (Santos et al., 2015), we be- in the recent past Serra del Molar was an iso- lieve it would be necessary to first carry out field lated island in front of the deltas of the Vinalopó surveys, with monitoring of individuals and ex- and Segura rivers (fig. 4a). Recently, the sedi- perimental studies to assess the C. ocellatus in- ments by both rivers settled and filled the area, teractions with the native biota, specifically the encircling Serra del Molar to the west and north skink C. bedriagai, as well as to perform eco- sides to form a lagoon environment of marshes, logical niche models that might hint on the fu- swamps and flood plains, which remained with ture distribution trends and possible expansion Human translocation of skinks across the Mediterranean Sea 11 of this species. The results of these proposed Amigues, S. (2004): Le silphium - État de la question. J. studies will help to evaluate the criteria in fu- Sçavans. 2: 191-226. Anderson, S.C. (1999): The Lizards of Iran. Society for the ture management for C. ocellatus in Serra del Study of Amphibians and Reptiles, New York. Molar. Aubet, M.E. (2009): Tiro y las colonias fenicias de Occi- Finally, new efforts are needed in the her- dente. Barcelona, Editorial Bellatera. petofaunal studies in archaeological contexts Azuar, R. (1998): Espacio hidráulico y ciudad islámica en el Vinalopó. La huerta de Elche. In: Agua y Territo- of the Iberian Mediterranean regions. The cur- rio. I Congreso de Estudios del Vinalopó. Volumen 2, rently known data show that the first records of p. 11-32. Rico, M.C., Ed., Centro de Estudios Locales some Maghrebian species in the Iberian Penin- del Vinalopó, Petrer. Azuar, R. (2016): Arqueología de las rutas, pecios y sula are dated in recent chronology, during the fondeaderos islámicos de las costas de Tudmîr (ss. VIII- Holocene (Bisbal-Chinesta and Blain, 2018). XIII). Tudmir 4: 7-26. Paleo-Archaeoherpetology can help us to iden- Baha El Din, S. (2006): A Guide to the Reptiles and Amphibians of Egypt. The American University in Cairo tify their arrival and the influences of the human Press, Cairo. factor on them. BDB-GVA (2018): Banc de Dades de Biodiversitat. Con- selleria d’Agricultura, Medi Ambient, Canvi Climàtic i Desenvolupament Rural, Generalitat Valenciana. http:// www.bdb.gva.es/lista-patron [Accessed 07.21.2018]. Acknowledgements. We are very grateful to the Editor Se- Beddek, M., Zenboudji-Beddek, S., Geniez, P., Fathalla, bastian Steinfartz, associated editor and four anonymous re- R., Sourouille, P., Arnal, V., Dellaoui, B., Koudach, F., viewers for their constructive comments on earlier draft of Telailia, S., Peyre, O., Crochet, P.A. (2018): Compara- this manuscript. The authors thank the staffs of the Wildlife Recovery Center La Granja del Saler of València city and tive phylogeography of amphibians and reptiles in Al- Santa Faç of Alacant for all their assistance as well as to geria suggests common causes for the east-west phylo- the herpetologists I. Lacomba and V. Sancho. F. Prados is geographic breaks in the Maghreb. PLoS One 13 (8): thanked for his constructive comments about Phoenician e0201218. colonization in southern Valencian Country. To Conselleria Berbegal, M.A. (2017): El Palmeral de Elche. Pasado, pre- de Medi Ambient of Generalitat Valenciana for the grant- sente y futuro. Aproximación antropológica. PhD dis- ing of faunistic prospecting permits (166/17FAU17_017, sertation. Departament de Ciències Socials i Humanes, 000/18FAU18_002). Finally, to our companions of the As- Universitat Miguel Hernández d’Elx. sociació Herpetològica Timon (AHT) during the surveys: Bisbal-Chinesta, J.F., Blain, H.-A. (2018): Long-term J. Burgos, E. Rosillo, M. Real, P. Luna, Á. Mondejar and changes in composition and distribution patterns in the E. Berdún. This paper is part of project CGL2016-80000- Iberian herpetofaunal communities since the latest Pleis- P of the Spanish Ministry of Economy and Competitive- tocene. Quat. Sci. Rev. 184: 143-166. ness and SGR2017-859 of the Generalitat de Catalunya. J.F. Blázquez, A.M. (2001): L’Albufera d’Elx. Evolución cua- Bisbal-Chinesta is supported by a FI Predoctoral Fellow- ternaria y reconstrucción paleoambiental a partir del es- ship 2016FI_B00286 with the financial sponsorship of the tudio de los foraminíferos fósiles. PhD dissertation. De- Agència de Gestió d’Ajuts Universitaris i de Recerca and partament de Geografia, Universitat de València. the Departament d’Empresa i Coneixement of the Generali- Blázquez, A.M., Usera, J. (2010): Palaeoenvironments and tat de Catalunya. S. Carranza and K. Tamar are supported by Quaternary foraminifera in the Elx coastal lagoon (Ali- project CGL2015-70390-P of the Spanish Ministry of Econ- cante, Spain). Quat. Int. 221 (1-2): 68-90. omy and Competitiveness (cofunded by FEDER). Buxó, R. (2008): The agricultural consequences of colonial contacts on the Iberian Peninsula in the first millennium B.C. Veg. Hist. Archaeobot. 17 (1): 145-154. Caputo, V., Guarino, F.M., Baldanza, F. (1997): A new Supplementary material. Supplementary material is avail- finding of the skink, Chalcides ocellatus, in the ex-royal able online at: garden of Portici (Naples, Italy). Bol. Asoc. Herpetol. https://doi.org/10.6084/m9.figshare.9703460 Esp. 8:3-4. Carranza, C., Arnold, E.N., Geniez, P., Roca, J., Mateo, J.A. (2008): Radiation, multiple dispersal and parallelism in References the skinks, Chalcides and Sphenops (Squamata: Scinci- dae), with comments on Scincus and Scincopus and the AHE (2018): Base de datos de anfibios y reptiles de Es- age of the Sahara Desert. Mol. Phylogenet. Evol. 46 (3): paña. Asociación Herpetológica Española. http://siare. 1071-1094. herpetologica.es [Accessed 07.20.2018]. Carranza, S., Arnold, E.N. (2006): Systematics, biogeog- Almela, A., Quintero, I., García, E., Mansilla, H. (1978): raphy, and evolution of Hemidactylus geckos (Reptilia: Guardamar del Segura. Segunda Serie, Primera Edición. Gekkonidae) elucidated using mitochondrial DNA se- Instituto Geológico y Minero de España, Madrid. quences. Mol. Phylogenet. Evol. 38: 531-545. 12 J.F. Bisbal-Chinesta et al.

Casson, L. (1989): The Periplus Maris Erythraei, Text With Insacco, G., Spadola, F., Russotto, S., Scaravelli, D. (2015): Introduction, Translation and Commentary. Princeton Eryx jaculus (Linnaeus, 1758): a new species for the Ital- University Press, Princeton. ian herpetofauna (Squamata: Erycidae). Acta Herpetol. Çiçek, K., Göçmen, B. (2013): Food consumption of Ocel- 10 (2): 149-153. lated Skink, Chalcides ocellatus (Forskal, 1775) (Squa- Iriarte, M.J., Ocete, C.A., Hernández, B., Ocete, R. (2016): mata: Scincidae), from the Cyprus Island. Acta Her- Vitis vinifera in the Iberian Peninsula: a review. Plant petol. 8 (2): 167-170. Biosyst. 151 (2): 245-257. Darriba, D., Taboada, G.L., Doallo, R., Posada, D. (2012): Karunarathna, D.M.S.S., Wickramasinghe, L.J.M., Sama- jModelTest 2: more models, new heuristics and parallel rawickrama, V.A.P., Munindradasa, D.A.I. (2009): The computing. Nat. Methods 9: 772-772. range extension of genus Chalcides Laurenti, 1768 Doménech, C. (2010): Los objetos egipcios y egiptizantes (Reptilia: Scincidae) to Sri Lanka. Russ. J. Herpetol. 15 en la protohistoria de Alicante. In: Objetos Egipcios (3): 225-228. en Alicante, p. 15-43. Olcina, M.H., Ramón, J.J., Eds, Katoh, K., Standley, D.M. (2013): MAFFT multiple se- Diputació d’Alacant, Alacant. quence alignment software version 7: improvements in Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A. performance and usability. Mol. Biol. Evol. 30: 772-780. (2012): Bayesian phylogenetics with BEAUti and the Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., BEAST 1.7. Mol. Biol. Evol. 29: 1969-1973. Pääbo, S., Villablanca, F.X., Wilson, A.C. (1989): Dy- Escolano, M. (2012): Egipto en la Península Ibérica: análi- namics of mitochondrial DNA evolution in animals: am- sis de siete amuletos del yacimiento fenicio de La plification and sequencing with conserved primers. Proc. Fonteta (Alicante). In: EPI OINOPA PONTON. Studi Natl. Acad. Sci. USA 86 (16): 6196-6200. sul Mediterraneo Antico in Ricordo di Giovanni Tore, Kolbe, J.J., Glor, R.E., Rodríguez-Schettino, L., Chamizo- p. 579-586. Del Vais, C., Ed., S’Alvure, Oristano. Lara, A., Larson, A., Losos, J.B. (2007): Multiple Ferry, M., Gómez, S. (2002): The Red Palm Weevil in the sources, admixture, and genetic variation in introduced Mediterranean Area. Palms 46 (4): 172-178. Anolis lizard populations. Conserv. Biol. 21 (6): 1612- Fitter, R.S.R. (1959): The Ark in Our Midst: the Story of the 1625. Introduced Animals of Britain; Birds, Beasts, Reptiles, Kornilios, P., Kyriazi, P., Poulakakis, N., Kumluta¸s, Y., Amphibians, Fishes. Collins, London. Ilgaz, Ç., Mylonas, M., Lymberakis, P. (2010): Phy- González, A. (2010a): La presencia fenicia en el Bajo Se- logeography of the ocellated skink Chalcides ocella- gura. In: Guardamar del Segura, Arqueología y Museo: tus (Squamata, Scincidae), with the use of mtDNA se- museos municipales en el MARQ, p. 58-65. García, A., quences: a hitch-hiker’s guide to the Mediterranean. Ed., Diputació d’Alacant, Guardamar del Segura. Mol. Phylogenet. Evol. 54: 445-456. González, A. (2010b): La colonia fenicia de la Fonteta. In: Kornilios, P., Thanou, E. (2016): Two additions to the Guardamar del Segura, Arqueología y Museo: museos herpetofauna of Kasos (Aegean Sea, Greece) and the municipales en el MARQ, p. 66-79. García, A., Ed., role of human-mediated dispersals. Herpetol. Rev. 47 Diputació d’Alacant, Guardamar del Segura. (4): 633-635. González, A. (2014): Útiles y objetos suntuosos. In: La Fonteta-2. Estudio de los materiales arqueológicos halla- Kraus, F. (2009): Alien Reptiles and Amphibians: a Scien- dos en la colonia fenicia de la actual desembocadura del tific Compendium and Analysis. Springer, Dordrecht. río Segura (Guardamar, Alicante), Volumen 1, p. 239- Krysko, K.L., Burgess, J.P., Rochford, M.R., Gillette, C.R., 245. González, A., Ed., Semanarios Internacionales so- Cueva, D., Enge, K.M., Somma, L.A., Stabile, J.L., bre Temas Fenicios, Alacant. Smith, D.C., Wasilewski, J.A., Kieckhefer III, G.N., Grau, I., Moratalla, J. (2001): Interpretación socioe- Granatrosky, M.C., Nielsen, S.V. (2011): Verified non- conómica del enclave. In: Poblamiento ibérico en el Bajo indigenous amphibians and reptiles in Florida from 1863 Segura. El Oral (II) y La Escuera, p. 173-204. Abad, L., through 2010: outlining the invasion process and identi- Sala-Sellés, F., Eds, Universitat d’Alacant, Alacant. fying invasion pathways and stages. Zootaxa 3028:1-6. Guindon, S., Gascuel, O. (2003): A simple, fast, and accu- Lavin, B.R., Papenfuss, T.J. (2012): The phylogenetic posi- rate algorithm to estimate large phylogenies by maxi- tion of Chalcides ocellatus (Squamata: Scincidae) from mum likelihood. Syst. Biol. 52: 696-704. Yemen and Somalia. Zootaxa 3221: 26-36. Gunn, J., Bowker, R., Sullivan, K.O., Sullivan, B. (2012): Lo Cascio, P., Grita, F. (2016): Introduzione accidentale di An Old World skink, Chalcides ocellatus, with a long gongilo Chalcides ocellatus (Forskal, 1775) (Squamata history of anthropogenically assisted dispersal, now es- Scincidae) nell’isola di Stromboli (Arcipelago Eoliano). tablished in Mesa, Arizona, USA. Herpetol. Rev. 43 (4): Natur. Sicil. 40 (2): 325-328. 551-553. López, M.J., Velázquez, F. (2012): Amuletos-placa de Gutiérrez, S. (1996): La cora de Tudm¯ır, de la antigüedad iconografía egipcia: El modelo vaca/udjat en el ámbito tardía al mundo islámico: poblamiento y cultura mate- fenicio-púnico. Cuad. Prehist. Arqueol. UAM 37-38: rial. École des Hautes Études Hispaniques, Madrid. 509-523. Harris, D.J., Batista, V., Lymberakis, P., Carretero, M.A. Lupo, S., Kohe, K. (2010): La integración de Tell El-Ghaba (2004): Complex estimates of evolutionary relationships al circuito comercial del Levante y el Mediterráneo in Tarentola mauritanica (Reptilia: Gekkonidae) derived Oriental entre los siglos VII y VI a.C. a través del estudio from mitochondrial DNA sequence. Mol. Phylogenet. de su cerámica importada. Rev. Inst. Hist. Ant. Or. 16: Evol. 30: 855-859. 27-52. Human translocation of skinks across the Mediterranean Sea 13

Martín, J., Mateus, C., García-Roa, R., Ortega, J., Carranza, Recuero, E., Iraola, A., Rubio, X., Marchodom, A., García, S. (2017): Phylogenetic relationships of the Chalcides M. (2007): Mitochondrial differentiation and biogeogra- skink species from the Chafarinas Islands with those phy of Hyla meridionalis (Anura: Hylidae): an unusual from mainland North Africa. Biochem. Syst. Ecol. 71: phylogeographical pattern. J. Biogeogr. 34: 1207-1219. 187-192. Rivas-Martínez, S. (1987): Memoria del Mapa de series Martínez, I., Vilaplana, E. (2014): Cuentas de collar de de vegetación de España 1:400.000. Instituto para la La Fonteta y La Peña Negra: descripción y análisis Conservación de la Naturaleza, Madrid. instrumental. In: La Fonteta-2. Estudio de los materiales Sánchez-Gómez, P., Jiménez, J.F., Vera, J.B., Sánchez- arqueológicos hallados en la colonia fenicia de la actual Saorín, F.J., Martínez, J.F., Buhagiar, J. (2013): Genetic desembocadura del río Segura (Guardamar, Alicante), structure of Tetraclinis articulata, an endangered conifer Volumen 2, p. 848-931. González, A., Ed., Semanarios of the western Mediterranean basin. Silva Fennica 45 Internacionales sobre Temas Fenicios, Alacant. (5): 1073. https://doi.org/10.14214/sf.1073. Masseti, M., Zuffi, M.A.L. (2011): Hypotheses on the origin Santos, J.L., Žagar, A., Drašler, K., Rato, C., Ayres, C., of the population of asp viper, Vipera aspis hugyi Schinz, Harris, D.J., Carretero, M.A., Salvi, D. (2019): Phylo- 1833, of the island of Montecristo, in the Northern geographic evidence for multiple long distance introduc- Tyrrhenian Sea (Tuscan archipelago, Italy). Br. Herpetol. tions of the common wall lizard associated with human Bull. 117:1-9. trade and transport. Amphib-Reptil. 40 (1): 121-127. Padró, J. (1975): Los objetos de tipo egipcio de la necrópo- Santos, X., Ayllón, E., Arribas, O., Bertolero, A., Bosch, lis de “El Molar” (Sant Fulgenci, Alicante) y su prob- J., Cabido, J., Carranza, S., Carretero, M.A., Díaz- lemática. Cuad. Prehist. Arqueo. Cast. 2: 133-142. Paniagua, C., Egea-Serrano, A., Garin-Barrio, I., Paulo, O.S., Pinto, I., Bruford, M.W., Jordan, W.C., Nichols, Giménez, A., Gosá, A., Graciá, E., Guicking, D., R.A. (2002): The double origin of Iberian Peninsular Llorente, G.A., Martínez-Solano, I., Mateo, J.A., Mon- chamaeleons. Biol. J. Linn. Soc. Lond. 75:1-7. tori, A., Palomar, G., Perera, A., Pinya, S., Petrus, J.L., Pfeiffer, S. (2010): Naukratis, Heracleion-Thonis and Pujol-Buxó, E., Rato, C., Recuero, E., Sanz-Azkue, I., Alexandria - Remarks on the presence and trade activ- Silva-Rocha, I., Vasconcelos, R., Velo-Antón, G., Vörös, ities of Greeks in the north-west Delta from the sev- J., Pleguezuelos, J.M. (2015): Síntesis de las introduc- enth century BC to the end of the fourth century BC. In: ciones de anfibios y reptiles en España. Bol. Asoc. Her- Alexandria and the North-Western Delta. Joint Confer- petol. Esp. 26 (2): 98-108. ence Proceedings of Alexandria: City and Harbour (Ox- Schleich, H.H., Kästle, W., Kabisch, K. (1996): Amphibians ford 2004) and the Trade and Topography of Egypt’s and Reptiles of North Africa. Koeltz Science Books, North-West Delta, 8th Century BC to 8th Century AD Koenigstein. (Berlin 2006), p. 15-24. Robinson, D., Wilson, A., Eds, Schneider, B. (1981): Chalcides ocellatus, Forsskål 1775 – Institute of Archaeology, Oxford. Walzenskink. In: Handbuch der Reptilien und Amphi- Pinya, S., Carretero, M.A. (2011): The Balearic herpeto- bien Europas, p. 338-354. Bohme, W., Ed., Aula Verlag, fauna: a species update and a review on the evidence. Wiesbaden. Acta Herpetol. 6: 59-80. Siépi, G. (1913): Adaptation du Gongyle ocellé, au territoire Pleguezuelos, J.M., Fahd, S., Carranza, S. (2008): El papel de Marseille. La Feuille des Jeunes Naturalistes 511: del Estrecho de Gibraltar en la conformación de la 114. actual fauna de anfibios y reptiles en el Mediterráneo Silva-Rocha, I., Montes, E., Salvi, D., Sillero, N., Mateo, Occidental. Bol. Asoc. Herpetol. Esp. 19: 2-17. J.A., Ayllón, E., Pleguezuelos, J.M., Carretero, M.A. Pooley, S., Queiroz, A.I. (2018): Introduction: historical (2018): Herpetological history of the Balearic islands: perspectives on bioinvasions in the Mediterranean re- when aliens conquered these islands and what to do gion. In: Histories of Bioinvasions in the Mediterranean, next. In: Histories of Bioinvasions in the Mediterranean, p. 1-19. Queiroz, A., Pooley, S., Eds, Springer, Cham. p. 105-131. Queiroz, A., Pooley, S., Eds, Springer, Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J. Cham. (2014): Tracer v1.6. Available at http://beast.bio.ed.ac. Silvestro, D., Michalak, I. (2012): RaxmlGUI: a graphical uk/Tracer. front-end for RAxML. Org. Divers. Evol. 12: 335-337. Rambaut, A., Drummond, A.J. (2010): FigTree v1.3.1. Spilani, L., Strachinis, I., Lampropoulos, A., Tsigas, P., Institute of Evolutionary Biology. University of Ed- Poulakakis, N., Pafilis, P. (2018): Podarcis vaucheri inburgh, UK. Available at: http://tree.bio.ed.ac.uk/ (Sauria: Lacertidae) far away from home: a new invasive software/figtree/. species in Greece. Amphib-Reptil. 39 (3): 363-368. Rato, C., Carranza, S., Harris, D.J. (2011): When selec- Stanley, J.D., Bernasconi, M.P., Jorstad, T.F. (2008): Pelu- tion deceives phylogeographic interpretation: the case of sium, an ancient port fortress on Egypt’s Nile delta coast: the Mediterranean house gecko (Hemidactylus turcicus) its evolving environmental setting from foundation to (Linnaeus, 1758). Mol. Phylogenet. Evol. 58: 365-373. demise.J.Coast.Res.24 (2): 451-462. Rato, C., Harris, D.J., Carranza, S., Machado, L., Perera, Stöck, M., Griffoni, G., Amor, N., Scheidt, U., Sicilia, A., A. (2016): The taxonomy of the Tarentola mauritanica Novarini, N. (2016): On the origin of the recent herpeto- species complex (Gekkota: Phyllodactylidae): Bayesian fauna of Sicily: comparative phylogeography using ho- species delimitation supports six candidate species. Mol. mologous mitochondrial and nuclear genes. Zool. Anz. Phylogenet. Evol. 94: 271-278. 261: 70-81. 14 J.F. Bisbal-Chinesta et al.

Tent-Manclús, J.E. (2012): Modelización del cambio de la Vallvé, J. (1999): Al-Ándalus: sociedad e instituciones. Real línea de costa en la comarca del Bajo Segura (Sinus Academia de la Historia, Madrid. Ilicitanus, S Provincia de Alicante) en los últimos 15.000 años. Cidaris 31: 55-62. Valenzuela, A., Cau, M.A., Alcover, J.A. (2016): Archaeo- Submitted: May 14, 2019. Final revision received: logical evidence for the introduction of Emys orbicularis (Testudines: Emydidae) in the Balearic islands, western July 12, 2019. Accepted: August 22, 2019. Mediterranean. Amphib-Reptil. 37 (2): 229-236. Associate Editor: Matthias Stöck. Amphibia-Reptilia Trade and stowaways: molecular evidence for human-

mediated translocation of eastern skinks into the western

Mediterranean

Josep Francesc Bisbal-Chinesta1,2,8,*, Karin Tamar3, Ángel Gálvez4,8, Luís Albero5,8,

Pablo Vicent-Castelló6,8, Laura Martín-Burgos7, Miguel Alonso8, Rubén Sánchez8,

Carlos Ortega8, Antonio Gómez8, David Candel8, Miguel Cervera8, Salvador Carranza3,

Hugues-Alexandre Blain1,2

1 - Unitat de Paleontologia, Institut Català de Paleoecologia Humana i Evolució Social (IPHES), Edifici

W3, Zona Educacional 4, Campus Sescelades, Universitat Rovira i Virgili, 43007 Tarragona, Spain

2 - Àrea de Prehistòria, Departament d’Història i Història de l’Art, Facultat de Lletres, Universitat Rovira i Virgili (URV), Avinguda de Catalunya 35, 43002 Tarragona, Spain

3 - Institute of Evolutionary Biology (IBE-CSIC/Universitat Pompeu Fabra), Passeig Marítim de la

Barceloneta, 37-49, 08003 Barcelona, Spain

4 - Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBiBE), Universitat de València. C/

Catedràtic José Beltrán Martínez 2, 46980 Paterna, València, Spain

5 - Área de Ecología, Departamento de Biodiversidad y Gestión Ambiental, Facultad de Ciencias

Biológicas, Universidad de León (ULE). Callejón Campus Vegazana s/n, 24071 León, Spain

6 - Museo Nacional de Ciencias Naturales (MNCN-CSIC), C/ José Gutiérrez Abascal 2, 28006 Madrid,

Spain

7 - EMCUJU Archaeologist, Ayuntamiento de Alpuente, C/ Rey Don Jaime 5, 46178 Alpuente, València,

Spain

8 - Secció de Estudis Científics, Associació Herpetològica Timon (AHT), C/ València 32, 46195 Llombai,

València, Spain

*Corresponding author; e-mail: [email protected]

Supplementary material

Table S1. Specimens used in the genetic analyses and related GenBank accession codes. Species Sample code Country cytb Reference C. ocellatus CN12564 Spain MN509445 This study C. ocellatus CN12645 Spain MN509446 This study C. ocellatus CN13391 Spain MN509447 This study C. ocellatus CN13434 Spain MN509448 This study C. ocellatus CN13435 Spain MN509449 This study Beddek et al., C. ocellatus BEV.11048 Algeria KY274233 2018 Beddek et al., C. ocellatus BEV.13254 Algeria KY274205 2018 Beddek et al., C. ocellatus BEV.13611 Algeria KY274209 2018 Beddek et al., C. ocellatus BEV.9200 Algeria KY274241 2018 Beddek et al., C. ocellatus BEV.9203 Algeria KY274243 2018 Beddek et al., C. ocellatus BEV.9227 Algeria KY274242 2018 Beddek et al., C. ocellatus BEV.9255 Algeria KY274247 2018 Beddek et al., C. ocellatus BEV.T1608 Algeria KY274234 2018 Beddek et al., C. ocellatus BEV.T1609 Algeria KY274235 2018 Beddek et al., C. ocellatus BEV.T4125 Algeria KY274236 2018 Beddek et al., C. ocellatus BEV.T4216 Algeria KY274250 2018 Beddek et al., C. ocellatus BEV.T4220 Algeria KY274237 2018 Beddek et al., C. ocellatus BEV.T4225 Algeria KY274238 2018 Beddek et al., C. ocellatus BEV.T4231 Algeria KY274239 2018

Species Sample code Country cytb Reference Beddek et al., C. ocellatus BEV.T4242 Algeria KY274240 2018 Beddek et al., C. ocellatus BEV.T633 Algeria KY274244 2018 Beddek et al., C. ocellatus BEV.T635 Algeria KY274245 2018 Beddek et al., C. ocellatus BEV.T637 Algeria KY274246 2018 Beddek et al., C. ocellatus BEV.T6500 Algeria KY274248 2018 Beddek et al., C. ocellatus BEV.T6839 Algeria KY274249 2018 Beddek et al., C. ocellatus BEV.T7918 Algeria KY274229 2018 Beddek et al., C. ocellatus BEV.T8026 Algeria KY274228 2018 Beddek et al., C. ocellatus BEV.T8027 Algeria KY274227 2018 Beddek et al., C. ocellatus BEV.T8028 Algeria KY274226 2018 Beddek et al., C. ocellatus BEV.T8029 Algeria KY274225 2018 Beddek et al., C. ocellatus BEV.T8030 Algeria KY274224 2018 Beddek et al., C. ocellatus BEV.T8031 Algeria KY274223 2018 Beddek et al., C. ocellatus BEV.T8032 Algeria KY274222 2018 Beddek et al., C. ocellatus BEV.T8033 Algeria KY274221 2018 Beddek et al., C. ocellatus BEV.T8034 Algeria KY274220 2018 Beddek et al., C. ocellatus BEV.T8035 Algeria KY274219 2018

Species Sample code Country cytb Reference Beddek et al., C. ocellatus BEV.T8037 Algeria KY274211 2018 Beddek et al., C. ocellatus BEV.T8038 Algeria KY274218 2018 Beddek et al., C. ocellatus BEV.T8039 Algeria KY274217 2018 Beddek et al., C. ocellatus BEV.T8041 Algeria KY274216 2018 Beddek et al., C. ocellatus BEV.T8042 Algeria KY274215 2018 Beddek et al., C. ocellatus BEV.T8043 Algeria KY274214 2018 Beddek et al., C. ocellatus BEV.T8044 Algeria KY274213 2018 Beddek et al., C. ocellatus BEV.T8045 Algeria KY274212 2018 Beddek et al., C. ocellatus BEV.T8064 Algeria KY274230 2018 Beddek et al., C. ocellatus BEV.T9407 Algeria KY274231 2018 Beddek et al., C. ocellatus BEV.T9548 Algeria KY274210 2018 Beddek et al., C. ocellatus BEV.T9580 Algeria KY274208 2018 Chafarinas C. ocellatus CN10018 KY614282 Martín et al., 2017 Islands Chafarinas C. ocellatus CN10019 KY614281 Martín et al., 2017 Islands Chafarinas C. ocellatus CN10020 KY614280 Martín et al., 2017 Islands Kornilios et al., C. ocellatus co10 Tunisia FJ980213 2010 Kornilios et al., C. ocellatus co13 Tunisia FJ980214 2010

Species Sample code Country cytb Reference Kornilios et al., C. ocellatus co14 Libya FJ980215 2010 Kornilios et al., C. ocellatus co16 Tunisia FJ980216 2010 Kornilios et al., C. ocellatus co25 Italy FJ980217 2010 Kornilios et al., C. ocellatus co29 Libya FJ980218 2010 Kornilios et al., C. ocellatus co30 Libya FJ980219 2010 Kornilios et al., C. ocellatus co31 Libya FJ980220 2010 Kornilios et al., C. ocellatus co33 Libya FJ980221 2010 Kornilios et al., C. ocellatus co34 Libya FJ980222 2010 Kornilios et al., C. ocellatus co35 Libya FJ980223 2010 Kornilios et al., C. ocellatus co36 Libya FJ980224 2010 Kornilios et al., C. ocellatus co37 Libya FJ980225 2010 Kornilios et al., C. ocellatus co38 Libya FJ980226 2010 Kornilios et al., C. ocellatus co39 Libya FJ980227 2010 Kornilios et al., C. ocellatus co41 Libya FJ980228 2010 Kornilios et al., C. ocellatus co42 Libya FJ980229 2010 Kornilios et al., C. ocellatus co43 Libya FJ980230 2010 Kornilios et al., C. ocellatus co44 Libya FJ980231 2010

Species Sample code Country cytb Reference Kornilios et al., C. ocellatus co45 Libya FJ980232 2010 Kornilios et al., C. ocellatus co46 Libya FJ980233 2010 Kornilios et al., C. ocellatus co47 Libya FJ980234 2010 Kornilios et al., C. ocellatus co48 Egypt FJ980235 2010 Kornilios et al., C. ocellatus co49 Egypt FJ980236 2010 Kornilios et al., C. ocellatus co50 Egypt FJ980237 2010 Kornilios et al., C. ocellatus co51 Egypt FJ980238 2010 Kornilios et al., C. ocellatus co52 Egypt FJ980239 2010 Kornilios et al., C. ocellatus co53 Egypt FJ980240 2010 Kornilios et al., C. ocellatus co60 Syria FJ980241 2010 Kornilios et al., C. ocellatus co61 Syria FJ980242 2010 Kornilios et al., C. ocellatus co63 Syria FJ980243 2010 Kornilios et al., C. ocellatus co64 Syria FJ980244 2010 Kornilios et al., C. ocellatus co65 Turkey FJ980245 2010 Kornilios et al., C. ocellatus co66 Turkey FJ980246 2010 Kornilios et al., C. ocellatus co67 Turkey FJ980247 2010 Kornilios et al., C. ocellatus co68 Turkey FJ980248 2010

Species Sample code Country cytb Reference Kornilios et al., C. ocellatus co69 Turkey FJ980249 2010 Kornilios et al., C. ocellatus co74 Turkey FJ980250 2010 Kornilios et al., C. ocellatus co75 Turkey FJ980251 2010 Kornilios et al., C. ocellatus co77 Cyprus FJ980253 2010 Kornilios et al., C. ocellatus co80 Cyprus FJ980254 2010 Kornilios et al., C. ocellatus co81 Cyprus FJ980255 2010 Kornilios et al., C. ocellatus co84 Cyprus FJ980256 2010 Kornilios et al., C. ocellatus co85 Cyprus FJ980257 2010 Kornilios et al., C. ocellatus co88 Greece FJ980258 2010 Kornilios et al., C. ocellatus co89 Greece FJ980259 2010 Kornilios et al., C. ocellatus co90 Greece FJ980260 2010 Kornilios et al., C. ocellatus co91 Greece FJ980261 2010 Kornilios et al., C. ocellatus co92 Greece FJ980262 2010 Kornilios et al., C. ocellatus co93 Greece FJ980263 2010 Kornilios et al., C. ocellatus co94 Greece FJ980264 2010 Kornilios et al., C. ocellatus co95 Greece FJ980265 2010 Kornilios et al., C. ocellatus co98 Greece FJ980266 2010

Species Sample code Country cytb Reference Kornilios et al., C. ocellatus co99 Greece FJ980267 2010 Kornilios et al., C. ocellatus co100 Greece FJ980268 2010 Kornilios et al., C. ocellatus co101 Greece FJ980269 2010 Kornilios et al., C. ocellatus co102 Greece FJ980270 2010 Carranza et al., C. ocellatus E04045.2 Israel EU278182 2008 Carranza et al., C. ocellatus E04045.4 Israel EU278183 2008 Carranza et al., C. ocellatus E04045.5 Israel EU278184 2008 Carranza et al., C. ocellatus E0602.2 Algeria EU278169 2008 Carranza et al., C. ocellatus E0602.9 Morocco EU278164 2008 Carranza et al., C. ocellatus E1009.1 Egypt EU278181 2008 Carranza et al., C. ocellatus E1009.2 Egypt EU278179 2008 Carranza et al., C. ocellatus E1009.3 Egypt EU278177 2008 Carranza et al., C. ocellatus E1906.1 Morocco EU278170 2008 Carranza et al., C. ocellatus E1906.2 Morocco EU278171 2008 Carranza et al., C. ocellatus E1906.3 Tunisia EU278194 2008 Carranza et al., C. ocellatus E1906.4 Tunisia EU278195 2008 Carranza et al., C. ocellatus E1906.5 Tunisia EU278196 2008

Species Sample code Country cytb Reference Carranza et al., C. ocellatus E1906.6 Tunisia EU278193 2008 Carranza et al., C. ocellatus E1906.7 Tunisia EU278198 2008 Carranza et al., C. ocellatus E1906.8 Tunisia EU278199 2008 Carranza et al., C. ocellatus E1906.9 Egypt EU278178 2008 Carranza et al., C. ocellatus E2002.1 Mauritania EU278173 2008 Carranza et al., C. ocellatus E2002.2 Mauritania EU278174 2008 Carranza et al., C. ocellatus E2006.1 Morocco EU278165 2008 Carranza et al., C. ocellatus E2006.10 Morocco EU278166 2008 Carranza et al., C. ocellatus E2006.12 Morocco EU278163 2008 Carranza et al., C. ocellatus E2006.13 Morocco EU278167 2008 Carranza et al., C. ocellatus E2006.14 Tunisia EU278188 2008 Carranza et al., C. ocellatus E2006.15 Tunisia EU278190 2008 Carranza et al., C. ocellatus E2006.17 Tunisia EU278189 2008 Carranza et al., C. ocellatus E2006.18 Tunisia EU278191 2008 Carranza et al., C. ocellatus E2006.19 Tunisia EU278197 2008 Carranza et al., C. ocellatus E2006.2 Morocco EU278168 2008 Carranza et al., C. ocellatus E2006.3 Cyprus EU278175 2008

Species Sample code Country cytb Reference Carranza et al., C. ocellatus E2006.4 Cyprus EU278176 2008 Carranza et al., C. ocellatus E2006.5 Italy EU278185 2008 Carranza et al., C. ocellatus E2006.7 Italy EU278187 2008 Carranza et al., C. ocellatus E2006.8 Italy EU278186 2008 Carranza et al., C. ocellatus E2006.9 Malta EU278192 2008 Carranza et al., C. ocellatus E2411.18 Turkey EU278180 2008 Carranza et al., C. ocellatus E2411.19 Egypt EU278172 2008 Lavin and C. ocellatus MVZ:235722 Tunisia JQ344285 Papenfuss, 2012 Lavin and C. ocellatus MVZ:235723 Tunisia JQ344284 Papenfuss, 2012 Lavin and C. ocellatus MVZ:235724 Algeria JQ344286 Papenfuss, 2012 Lavin and C. ocellatus MVZ:236589 Yemen JQ344283 Papenfuss, 2012 Lavin and C. ocellatus MVZ:239220 Turkey JQ344282 Papenfuss, 2012 Lavin and C. ocellatus MVZ:242790 Somalia JQ344290 Papenfuss, 2012 Kornilios et al., C. montanus co103 Morocco FJ980271 2010 Kornilios et al., C. montanus co104 Morocco FJ980272 2010

Figure S1. Cytochrome b Maximum likelihood phylogenetic tree of Chalcides ocellatus. Bootstrap (ML) and Bayesian posterior probabilities (BI) support values are indicated above and below the nodes, respectively. The newly discovered Spanish specimens collected from Serra Marina, Elx are highlighted. Sample codes and localities correlate to specimens in supplementary table S1.