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

In: Amphibia-Reptilia

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.

  • AHE (2018): Base de datos de anfibios y reptiles de España. Asociación Herpetológica Española. http://siare.herpetologica.es [Accessed 07.20.2018].

  • AlmelaA.QuinteroI.GarcíaE.MansillaH. (1978): Guardamar del Segura. Segunda Serie Primera Edición. Instituto Geológico y Minero de EspañaMadrid.

    • Search Google Scholar
    • Export Citation
  • AmiguesS. (2004): Le silphium - État de la question. J. Sçavans. 2: 191-226.

  • AndersonS.C. (1999): The Lizards of Iran. Society for the Study of Amphibians and ReptilesNew York.

  • AubetM.E. (2009): Tiro y las colonias fenicias de Occidente. Barcelona Editorial Bellatera.

  • AzuarR. (1998): Espacio hidráulico y ciudad islámica en el Vinalopó. La huerta de Elche. In: Agua y Territorio. I Congreso de Estudios del Vinalopó. Volumen 2 p. 11-32. RicoM.C. Ed. Centro de Estudios Locales del VinalopóPetrer.

    • Search Google Scholar
    • Export Citation
  • AzuarR. (2016): Arqueología de las rutas, pecios y fondeaderos islámicos de las costas de Tudmîr (ss. VIII-XIII). Tudmir 4: 7-26.

  • Baha El DinS. (2006): A Guide to the Reptiles and Amphibians of Egypt. The American University in Cairo PressCairo.

  • BDB-GVA (2018): Banc de Dades de Biodiversitat. Conselleria d’Agricultura Medi Ambient Canvi Climàtic i Desenvolupament Rural Generalitat Valenciana. http://www.bdb.gva.es/lista-patron [Accessed 07.21.2018].

  • BeddekM.Zenboudji-BeddekS.GeniezP.FathallaR.SourouilleP.ArnalV.DellaouiB.KoudachF.TelailiaS.PeyreO.CrochetP.A. (2018): Comparative phylogeography of amphibians and reptiles in Algeria suggests common causes for the east-west phylogeographic breaks in the Maghreb. PLoS One 13 (8): e0201218.

    • Search Google Scholar
    • Export Citation
  • BerbegalM.A. (2017): El Palmeral de Elche. Pasado presente y futuro. Aproximación antropológica. PhD dissertation. Departament de Ciències Socials i Humanes Universitat Miguel Hernández d’Elx.

  • Bisbal-ChinestaJ.F.BlainH.-A. (2018): Long-term changes in composition and distribution patterns in the Iberian herpetofaunal communities since the latest Pleistocene. Quat. Sci. Rev. 184: 143-166.

    • Search Google Scholar
    • Export Citation
  • BlázquezA.M. (2001): L’Albufera d’Elx. Evolución cuaternaria y reconstrucción paleoambiental a partir del estudio de los foraminíferos fósiles. PhD dissertation. Departament de Geografia Universitat de València.

  • BlázquezA.M.UseraJ. (2010): Palaeoenvironments and Quaternary foraminifera in the Elx coastal lagoon (Alicante, Spain). Quat. Int. 221 (1-2): 68-90.

    • Search Google Scholar
    • Export Citation
  • BuxóR. (2008): The agricultural consequences of colonial contacts on the Iberian Peninsula in the first millennium B.C. Veg. Hist. Archaeobot. 17 (1): 145-154.

    • Search Google Scholar
    • Export Citation
  • CaputoV.GuarinoF.M.BaldanzaF. (1997): A new finding of the skink, Chalcides ocellatus, in the ex-royal garden of Portici (Naples, Italy). Bol. Asoc. Herpetol. Esp. 8: 3-4.

    • Search Google Scholar
    • Export Citation
  • CarranzaC.ArnoldE.N.GeniezP.RocaJ.MateoJ.A. (2008): Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Mol. Phylogenet. Evol. 46 (3): 1071-1094.

    • Search Google Scholar
    • Export Citation
  • CarranzaS.ArnoldE.N. (2006): Systematics, biogeography, and evolution of Hemidactylus geckos (Reptilia: Gekkonidae) elucidated using mitochondrial DNA sequences. Mol. Phylogenet. Evol. 38: 531-545.

    • Search Google Scholar
    • Export Citation
  • CassonL. (1989): The Periplus Maris Erythraei Text With Introduction Translation and Commentary. Princeton University PressPrinceton.

    • Search Google Scholar
    • Export Citation
  • ÇiçekK.GöçmenB. (2013): Food consumption of Ocellated Skink, Chalcides ocellatus (Forskal, 1775) (Squamata: Scincidae), from the Cyprus Island. Acta Herpetol. 8 (2): 167-170.

    • Search Google Scholar
    • Export Citation
  • DarribaD.TaboadaG.L.DoalloR.PosadaD. (2012): jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772-772.

    • Search Google Scholar
    • Export Citation
  • DoménechC. (2010): Los objetos egipcios y egiptizantes en la protohistoria de Alicante. In: Objetos Egipcios en Alicante p. 15-43. OlcinaM.H.RamónJ.J. Eds Diputació d’AlacantAlacant.

    • Search Google Scholar
    • Export Citation
  • DrummondA.J.SuchardM.A.XieD.RambautA. (2012): Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29: 1969-1973.

    • Search Google Scholar
    • Export Citation
  • EscolanoM. (2012): Egipto en la Península Ibérica: análisis de siete amuletos del yacimiento fenicio de La Fonteta (Alicante). In: EPI OINOPA PONTON. Studi sul Mediterraneo Antico in Ricordo di Giovanni Tore p. 579-586. Del VaisC. Ed. S’AlvureOristano.

    • Search Google Scholar
    • Export Citation
  • FerryM.GómezS. (2002): The Red Palm Weevil in the Mediterranean Area. Palms 46 (4): 172-178.

  • FitterR.S.R. (1959): The Ark in Our Midst: the Story of the Introduced Animals of Britain; Birds Beasts Reptiles Amphibians Fishes. CollinsLondon.

    • Search Google Scholar
    • Export Citation
  • GonzálezA. (2010a): La presencia fenicia en el Bajo Segura. In: Guardamar del Segura Arqueología y Museo: museos municipales en el MARQ p. 58-65. GarcíaA. Ed. Diputació d’AlacantGuardamar del Segura.

    • Search Google Scholar
    • Export Citation
  • GonzálezA. (2010b): La colonia fenicia de la Fonteta. In: Guardamar del Segura Arqueología y Museo: museos municipales en el MARQ p. 66-79. GarcíaA. Ed. Diputació d’AlacantGuardamar del Segura.

    • Search Google Scholar
    • Export Citation
  • GonzálezA. (2014): Útiles y objetos suntuosos. In: La Fonteta-2. Estudio de los materiales arqueológicos hallados en la colonia fenicia de la actual desembocadura del río Segura (Guardamar Alicante) Volumen 1 p. 239-245. GonzálezA. Ed. Semanarios Internacionales sobre Temas FeniciosAlacant.

    • Search Google Scholar
    • Export Citation
  • GrauI.MoratallaJ. (2001): Interpretación socioeconómica del enclave. In: Poblamiento ibérico en el Bajo Segura. El Oral (II) y La Escuera p. 173-204. AbadL.Sala-SellésF. Eds Universitat d’AlacantAlacant.

    • Search Google Scholar
    • Export Citation
  • GuindonS.GascuelO. (2003): A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.

    • Search Google Scholar
    • Export Citation
  • GunnJ.BowkerR.SullivanK.O.SullivanB. (2012): An Old World skink, Chalcides ocellatus, with a long history of anthropogenically assisted dispersal, now established in Mesa, Arizona, USA. Herpetol. Rev. 43 (4): 551-553.

    • Search Google Scholar
    • Export Citation
  • GutiérrezS. (1996): La cora de Tudmı¯r de la antigüedad tardía al mundo islámico: poblamiento y cultura material. École des Hautes Études HispaniquesMadrid.

    • Search Google Scholar
    • Export Citation
  • HarrisD.J.BatistaV.LymberakisP.CarreteroM.A. (2004): Complex estimates of evolutionary relationships in Tarentola mauritanica (Reptilia: Gekkonidae) derived from mitochondrial DNA sequence. Mol. Phylogenet. Evol. 30: 855-859.

    • Search Google Scholar
    • Export Citation
  • InsaccoG.SpadolaF.RussottoS.ScaravelliD. (2015): Eryx jaculus (Linnaeus, 1758): a new species for the Italian herpetofauna (Squamata: Erycidae). Acta Herpetol. 10 (2): 149-153.

    • Search Google Scholar
    • Export Citation
  • IriarteM.J.OceteC.A.HernándezB.OceteR. (2016): Vitis vinifera in the Iberian Peninsula: a review. Plant Biosyst. 151 (2): 245-257.

    • Search Google Scholar
    • Export Citation
  • KarunarathnaD.M.S.S.WickramasingheL.J.M.SamarawickramaV.A.P.MunindradasaD.A.I. (2009): The range extension of genus Chalcides Laurenti, 1768 (Reptilia: Scincidae) to Sri Lanka. Russ. J. Herpetol. 15 (3): 225-228.

    • Search Google Scholar
    • Export Citation
  • KatohK.StandleyD.M. (2013): MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780.

    • Search Google Scholar
    • Export Citation
  • KocherT.D.ThomasW.K.MeyerA.EdwardsS.V.PääboS.VillablancaF.X.WilsonA.C. (1989): Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86 (16): 6196-6200.

    • Search Google Scholar
    • Export Citation
  • KolbeJ.J.GlorR.E.Rodríguez-SchettinoL.Chamizo-LaraA.LarsonA.LososJ.B. (2007): Multiple sources, admixture, and genetic variation in introduced Anolis lizard populations. Conserv. Biol. 21 (6): 1612-1625.

    • Search Google Scholar
    • Export Citation
  • KorniliosP.KyriaziP.PoulakakisN.KumlutaşY.IlgazÇ.MylonasM.LymberakisP. (2010): Phylogeography of the ocellated skink Chalcides ocellatus (Squamata, Scincidae), with the use of mtDNA sequences: a hitch-hiker’s guide to the Mediterranean. Mol. Phylogenet. Evol. 54: 445-456.

    • Search Google Scholar
    • Export Citation
  • KorniliosP.ThanouE. (2016): Two additions to the herpetofauna of Kasos (Aegean Sea, Greece) and the role of human-mediated dispersals. Herpetol. Rev. 47 (4): 633-635.

    • Search Google Scholar
    • Export Citation
  • KrausF. (2009): Alien Reptiles and Amphibians: a Scientific Compendium and Analysis. SpringerDordrecht.

  • KryskoK.L.BurgessJ.P.RochfordM.R.GilletteC.R.CuevaD.EngeK.M.SommaL.A.StabileJ.L.SmithD.C.WasilewskiJ.A.Kieckhefer IIIG.N.GranatroskyM.C.NielsenS.V. (2011): Verified non-indigenous amphibians and reptiles in Florida from 1863 through 2010: outlining the invasion process and identifying invasion pathways and stages. Zootaxa 3028: 1-6.

    • Search Google Scholar
    • Export Citation
  • LavinB.R.PapenfussT.J. (2012): The phylogenetic position of Chalcides ocellatus (Squamata: Scincidae) from Yemen and Somalia. Zootaxa 3221: 26-36.

    • Search Google Scholar
    • Export Citation
  • Lo CascioP.GritaF. (2016): Introduzione accidentale di gongilo Chalcides ocellatus (Forskal, 1775) (Squamata Scincidae) nell’isola di Stromboli (Arcipelago Eoliano). Natur. Sicil. 40 (2): 325-328.

    • Search Google Scholar
    • Export Citation
  • LópezM.J.VelázquezF. (2012): Amuletos-placa de iconografía egipcia: El modelo vaca/udjat en el ámbito fenicio-púnico. Cuad. Prehist. Arqueol. UAM 37-38: 509-523.

    • Search Google Scholar
    • Export Citation
  • LupoS.KoheK. (2010): La integración de Tell El-Ghaba al circuito comercial del Levante y el Mediterráneo Oriental entre los siglos VII y VI a.C. a través del estudio de su cerámica importada. Rev. Inst. Hist. Ant. Or. 16: 27-52.

    • Search Google Scholar
    • Export Citation
  • MartínJ.MateusC.García-RoaR.OrtegaJ.CarranzaS. (2017): Phylogenetic relationships of the Chalcides skink species from the Chafarinas Islands with those from mainland North Africa. Biochem. Syst. Ecol. 71: 187-192.

    • Search Google Scholar
    • Export Citation
  • MartínezI.VilaplanaE. (2014): Cuentas de collar de La Fonteta y La Peña Negra: descripción y análisis instrumental. In: La Fonteta-2. Estudio de los materiales arqueológicos hallados en la colonia fenicia de la actual desembocadura del río Segura (Guardamar Alicante) Volumen 2 p. 848-931. GonzálezA. Ed. Semanarios Internacionales sobre Temas FeniciosAlacant.

    • Search Google Scholar
    • Export Citation
  • MassetiM.ZuffiM.A.L. (2011): Hypotheses on the origin of the population of asp viper, Vipera aspis hugyi Schinz, 1833, of the island of Montecristo, in the Northern Tyrrhenian Sea (Tuscan archipelago, Italy). Br. Herpetol. Bull. 117: 1-9.

    • Search Google Scholar
    • Export Citation
  • PadróJ. (1975): Los objetos de tipo egipcio de la necrópolis de “El Molar” (Sant Fulgenci, Alicante) y su problemática. Cuad. Prehist. Arqueo. Cast. 2: 133-142.

    • Search Google Scholar
    • Export Citation
  • PauloO.S.PintoI.BrufordM.W.JordanW.C.NicholsR.A. (2002): The double origin of Iberian Peninsular chamaeleons. Biol. J. Linn. Soc. Lond. 75: 1-7.

    • Search Google Scholar
    • Export Citation
  • PfeifferS. (2010): Naukratis, Heracleion-Thonis and Alexandria - Remarks on the presence and trade activities of Greeks in the north-west Delta from the seventh century BC to the end of the fourth century BC. In: Alexandria and the North-Western Delta. Joint Conference Proceedings of Alexandria: City and Harbour (Oxford 2004) and the Trade and Topography of Egypt’s North-West Delta 8th Century BC to 8th Century AD (Berlin 2006) p. 15-24. RobinsonD.WilsonA. Eds Institute of ArchaeologyOxford.

    • Search Google Scholar
    • Export Citation
  • PinyaS.CarreteroM.A. (2011): The Balearic herpetofauna: a species update and a review on the evidence. Acta Herpetol. 6: 59-80.

  • PleguezuelosJ.M.FahdS.CarranzaS. (2008): El papel del Estrecho de Gibraltar en la conformación de la actual fauna de anfibios y reptiles en el Mediterráneo Occidental. Bol. Asoc. Herpetol. Esp. 19: 2-17.

    • Search Google Scholar
    • Export Citation
  • PooleyS.QueirozA.I. (2018): Introduction: historical perspectives on bioinvasions in the Mediterranean region. In: Histories of Bioinvasions in the Mediterranean p. 1-19. QueirozA.PooleyS. Eds SpringerCham.

    • Search Google Scholar
    • Export Citation
  • RambautA.SuchardM.A.XieD.DrummondA.J. (2014): Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer.

  • RambautA.DrummondA.J. (2010): FigTree v1.3.1. Institute of Evolutionary Biology. University of EdinburghUK. Available at: http://tree.bio.ed.ac.uk/software/figtree/.

    • Search Google Scholar
    • Export Citation
  • RatoC.CarranzaS.HarrisD.J. (2011): When selection deceives phylogeographic interpretation: the case of the Mediterranean house gecko (Hemidactylus turcicus) (Linnaeus, 1758). Mol. Phylogenet. Evol. 58: 365-373.

    • Search Google Scholar
    • Export Citation
  • RatoC.HarrisD.J.CarranzaS.MachadoL.PereraA. (2016): The taxonomy of the Tarentola mauritanica species complex (Gekkota: Phyllodactylidae): Bayesian species delimitation supports six candidate species. Mol. Phylogenet. Evol. 94: 271-278.

    • Search Google Scholar
    • Export Citation
  • RecueroE.IraolaA.RubioX.MarchodomA.GarcíaM. (2007): Mitochondrial differentiation and biogeography of Hyla meridionalis (Anura: Hylidae): an unusual phylogeographical pattern. J. Biogeogr. 34: 1207-1219.

    • Search Google Scholar
    • Export Citation
  • Rivas-MartínezS. (1987): Memoria del Mapa de series de vegetación de España 1:400.000. Instituto para la Conservación de la NaturalezaMadrid.

    • Search Google Scholar
    • Export Citation
  • Sánchez-GómezP.JiménezJ.F.VeraJ.B.Sánchez-SaorínF.J.MartínezJ.F.BuhagiarJ. (2013): Genetic structure of Tetraclinis articulata, an endangered conifer of the western Mediterranean basin. Silva Fennica 45 (5): 1073. https://doi.org/10.14214/sf.1073.

    • Search Google Scholar
    • Export Citation
  • SantosJ.L.ŽagarA.DrašlerK.RatoC.AyresC.HarrisD.J.CarreteroM.A.SalviD. (2019): Phylogeographic evidence for multiple long distance introductions of the common wall lizard associated with human trade and transport. Amphib-Reptil. 40 (1): 121-127.

    • Search Google Scholar
    • Export Citation
  • SantosX.AyllónE.ArribasO.BertoleroA.BoschJ.CabidoJ.CarranzaS.CarreteroM.A.Díaz-PaniaguaC.Egea-SerranoA.Garin-BarrioI.GiménezA.GosáA.GraciáE.GuickingD.LlorenteG.A.Martínez-SolanoI.MateoJ.A.MontoriA.PalomarG.PereraA.PinyaS.PetrusJ.L.Pujol-BuxóE.RatoC.RecueroE.Sanz-AzkueI.Silva-RochaI.VasconcelosR.Velo-AntónG.VörösJ.PleguezuelosJ.M. (2015): Síntesis de las introducciones de anfibios y reptiles en España. Bol. Asoc. Herpetol. Esp. 26 (2): 98-108.

    • Search Google Scholar
    • Export Citation
  • SchleichH.H.KästleW.KabischK. (1996): Amphibians and Reptiles of North Africa. Koeltz Science BooksKoenigstein.

  • SchneiderB. (1981): Chalcides ocellatus, Forsskål 1775 – Walzenskink. In: Handbuch der Reptilien und Amphibien Europas p. 338-354. BohmeW. Ed. Aula VerlagWiesbaden.

    • Search Google Scholar
    • Export Citation
  • SiépiG. (1913): Adaptation du Gongyle ocellé, au territoire de Marseille. La Feuille des Jeunes Naturalistes 511: 114.

  • Silva-RochaI.MontesE.SalviD.SilleroN.MateoJ.A.AyllónE.PleguezuelosJ.M.CarreteroM.A. (2018): Herpetological history of the Balearic islands: when aliens conquered these islands and what to do next. In: Histories of Bioinvasions in the Mediterranean p. 105-131. QueirozA.PooleyS. Eds SpringerCham.

    • Search Google Scholar
    • Export Citation
  • SilvestroD.MichalakI. (2012): RaxmlGUI: a graphical front-end for RAxML. Org. Divers. Evol. 12: 335-337.

  • SpilaniL.StrachinisI.LampropoulosA.TsigasP.PoulakakisN.PafilisP. (2018): Podarcis vaucheri (Sauria: Lacertidae) far away from home: a new invasive species in Greece. Amphib-Reptil. 39 (3): 363-368.

    • Search Google Scholar
    • Export Citation
  • StanleyJ.D.BernasconiM.P.JorstadT.F. (2008): Pelusium, an ancient port fortress on Egypt’s Nile delta coast: its evolving environmental setting from foundation to demise. J. Coast. Res. 24 (2): 451-462.

    • Search Google Scholar
    • Export Citation
  • StöckM.GriffoniG.AmorN.ScheidtU.SiciliaA.NovariniN. (2016): On the origin of the recent herpetofauna of Sicily: comparative phylogeography using homologous mitochondrial and nuclear genes. Zool. Anz. 261: 70-81.

    • Search Google Scholar
    • Export Citation
  • Tent-ManclúsJ.E. (2012): Modelización del cambio de la línea de costa en la comarca del Bajo Segura (Sinus Ilicitanus, S Provincia de Alicante) en los últimos 15.000 años. Cidaris 31: 55-62.

    • Search Google Scholar
    • Export Citation
  • ValenzuelaA.CauM.A.AlcoverJ.A. (2016): Archaeological evidence for the introduction of Emys orbicularis (Testudines: Emydidae) in the Balearic islands, western Mediterranean. Amphib-Reptil. 37 (2): 229-236.

    • Search Google Scholar
    • Export Citation
  • VallvéJ. (1999): Al-Ándalus: sociedad e instituciones. Real Academia de la HistoriaMadrid.

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 491 491 70
Full Text Views 24 24 4
PDF Downloads 9 9 2