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Organisms Diversity & Evolution

, Volume 14, Issue 3, pp 295–306 | Cite as

Where are you from, stranger? The enigmatic biogeography of North African pond turtles (Emys orbicularis)

  • Heiko Stuckas
  • Guillermo Velo-Antón
  • Soumia Fahd
  • Mohsen Kalboussi
  • Rachid Rouag
  • Marco Arculeo
  • Federico Marrone
  • Francesco Sacco
  • Melita Vamberger
  • Uwe FritzEmail author
Original Article

Abstract

The European pond turtle (Emys orbicularis) is a Nearctic element in the African fauna and thought to have invaded North Africa from the Iberian Peninsula. All North African populations are currently identified with the subspecies E. o. occidentalis. However, a nearly range-wide sampling in North Africa used for analyses of mitochondrial and microsatellite DNA provides evidence that only Moroccan populations belong to this taxon, while eastern Algerian and Tunisian pond turtles represent an undescribed distinct subspecies. These two taxa are most closely related to E. o. galloitalica with a native distribution along the Mediterranean coast of northern Spain through southern France to western and southern Italy. This group is sister to a clade comprising several mitochondrial lineages and subspecies of E. orbicularis from Central and Eastern Europe plus Asia, and the successive sisters are E. o. hellenica and E. trinacris. Our results suggest that E. orbicularis has been present in North Africa longer than on the Iberian Peninsula and that after an initial invasion of North Africa by pond turtles from an unknown European source region, there was a phase of diversification in North Africa, followed by a later re-invasion of Europe by one of the African lineages. The differentiation of pond turtles in North Africa parallels a general phylogeographic paradigm in amphibians and reptiles, with deeply divergent lineages in the western and eastern Maghreb. Acknowledging their genetic similarity, we propose to synonymize the previously recognized Iberian subspecies E. o. fritzjuergenobsti with E. o. occidentalis sensu stricto. The seriously imperiled Moroccan populations of E. o. occidentalis represent two Management Units different in mitochondrial haplotypes and microsatellite markers. The conservation status of eastern Algerian pond turtles is unclear, while Tunisian populations are endangered. Considering that Algerian and Tunisian pond turtles represent an endemic taxon, their situation throughout the historical range should be surveyed to establish a basis for conservation measures.

Keywords

Reptilia Testudines Emydidae Phylogeography Africa Iberian Peninsula Palaearctic 

Notes

Acknowledgements

Most of the laboratory work was done by Anke Müller. Special thanks go to Martin Päckert for the exploratory molecular clock calculations. Alessandra Sicilia assisted during fieldwork. Oscar Arribas, Massimo Delfino and Aitor Valdeón helped with references for fossils. Guillermo Velo-Antón’s research was supported by the Fundação para a Ciência e Tecnologia (SFRH/BPD/74834/2010).

Supplementary material

13127_2014_168_MOESM1_ESM.pdf (1.8 mb)
ESM 1 (PDF 1.81 MB)

References

  1. Bailón, S. (2011). Quelonios fósiles del yacimiento de Barranco León (Pleistoceno inferior, Orce, Granada, España). In I. Toro, B. Martínez-Navarro, & J. Agustí (Eds.), Ocupaciones humanas en el Pleistoceno inferior y medio de la Cuenca de Guadix-Baza (pp. 185–195). Sevilla: Junta de Andalucía, Consejería de Cultura.Google Scholar
  2. Blasco, R., Blain, H.-A., Rosell, J., Díez, J. C., Huguet, R., Rodríguez, J., Arsuaga, J. L., Bermúdez de Castro, J. M., & Carbonell, E. (2011). Earliest evidence for human consumption of tortoises in the European Early Pleistocene from Sima del Elefante, Sierra de Atapuerca, Spain. Journal of Human Evolution, 61, 503–509.PubMedCrossRefGoogle Scholar
  3. Bons, J., & Geniez, P. (1996). Amphibiens et reptiles du Maroc (Sahara Occidental compris). Atlas biogéographique. Barcelona: AHE.Google Scholar
  4. Carranza, S., & Arnold, E. N. (2004). History of West Mediterranean newts, Pleurodeles (Amphibia: Salamandridae), inferred from old and recent DNA sequences. Systematics and Biodiversity, 1, 327–337.CrossRefGoogle Scholar
  5. Carranza, S., Arnold, E. N., Wade, E., & Fahd, S. (2004). Phylogeography of the false smooth snakes, Macroprotodon (Serpentes, Colubridae): mitochondrial DNA sequences show European populations arrived recently from Northwest Africa. Molecular Phylogenetics and Evolution, 33, 523–532.PubMedCrossRefGoogle Scholar
  6. Carranza, S., Arnold, E. N., & Pleguezuelos, J. M. (2006). Phylogeny, biogeography, and evolution of two Mediterranean snakes, Malpolon monspessulanus and Hemorrhois hippocrepis (Squamata, Colubridae), using mtDNA sequences. Molecular Phylogenetics and Evolution, 40, 532–546.PubMedCrossRefGoogle Scholar
  7. Ciofi, C., Tzika, A. C., Natali, C., Chelazzi, G., Naziridis, T., & Milinkovitch, M. C. (2009). Characterization of microsatellite loci in the European pond turtle Emys orbicularis. Molecular Ecology Resources, 9, 189–191.PubMedCrossRefGoogle Scholar
  8. Clement, M., Posada, D., & Crandall, K. A. (2000). tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.PubMedCrossRefGoogle Scholar
  9. de Lapparent de Broin, F. (2000). African chelonians from the Jurassic to the present: phases of development and preliminary catalogue of the fossil record. Palaeontologia Africana, 36, 43–82.Google Scholar
  10. Delfino, M. (2002). Erpetofaune italiane del Neogene e del Quaternario. PhD thesis, Università degli Studi di Modena e Reggio Emilia.Google Scholar
  11. Dimaki, M., Hundsdörfer, A. K., & Fritz, U. (2008). Eastern Mediterranean chameleons (Chamaeleo chamaeleon, Ch. africanus) are distinct. Amphibia-Reptilia, 29, 535–540.CrossRefGoogle Scholar
  12. Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611–2620.PubMedCrossRefGoogle Scholar
  13. Excoffier, L., Laval, G., & Schneider, S. (2005). arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.PubMedCentralGoogle Scholar
  14. Fahd, S., El Marnisi, B., Mediani, M., & Fritz, U. (2009). Zur Verbreitung und zum Bedrohungsstatus der Europäischen Sumpfschildkröte (Emys orbicularis) in Marokko. Elaphe, 17, 30–33.Google Scholar
  15. Fritz, U. (1993). Zur innerartlichen Variabilität von Emys orbicularis (Linnaeus, 1758). 3. Zwei neue Unterarten von der Iberischen Halbinsel und aus Nordafrika, Emys orbicularis fritzjuergenobsti subsp. nov. und E. o. occidentalis subsp. nov. Zoologische Abhandlungen des Staatlichen Museums für Tierkunde Dresden, 47, 131–155.Google Scholar
  16. Fritz, U. (1994). Gibt es in Nordafrika zwei verschiedene Formen der Europäischen Sumpfschildkröte (Emys orbicularis)? Salamandra, 30, 76–80.Google Scholar
  17. Fritz, U. (1995). Kritische Übersicht der Fossilgeschichte der Sumpfschildkröten-Gattung Emys A. Duméril, 1806. Zoologische Abhandlungen des Staatlichen Museums für Tierkunde Dresden, 48, 243–264.Google Scholar
  18. Fritz, U. (1996). Zur innerartlichen Variabilität von Emys orbicularis (Linnaeus, 1758). 5b. Innerartliche Hierarchie und Zoogeographie. Zoologische Abhandlungen des Staatlichen Museums für Tierkunde Dresden, 49, 31–71.Google Scholar
  19. Fritz, U. (1998). Introduction to zoogeography and subspecific differentiation in Emys orbicularis (Linnaeus, 1758). Mertensiella, 10, 1–27.Google Scholar
  20. Fritz, U. (2001). Emys orbicularis (Linnaeus, 1758) – Europäische Sumpfschildkröte. In U. Fritz (Ed.), Handbuch der Reptilien und Amphibien Europas. Band 3/IIIA: Schildkröten I (pp. 343–515). Wiebelsheim: Aula-Verlag.Google Scholar
  21. Fritz, U. (2003). Die Europäische Sumpfschildkröte. Bielefeld: Laurenti.Google Scholar
  22. Fritz, U., & Havaš, P. (2007). Checklist of chelonians of the world. Vertebrate Zoology, 57, 149–368.Google Scholar
  23. Fritz, U., Guicking, D., Lenk, P., Joger, U., & Wink, M. (2004). When turtle distribution tells European history: mtDNA haplotypes of Emys orbicularis reflect in Germany former division by the Iron Curtain. Biologia, 59(Supplement 14), 19–25.Google Scholar
  24. Fritz, U., Fattizzo, T., Guicking, D., Tripepi, S., Pennisi, M. G., Lenk, P., Joger, U., & Wink, M. (2005). A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys. Zoologica Scripta, 34, 351–371.CrossRefGoogle Scholar
  25. Fritz, U., d’Angelo, S., Pennisi, M. G., & Lo Valvo, M. (2006a). Variation of Sicilian pond turtles, Emys trinacris – What makes a species cryptic? Amphibia-Reptilia, 27, 513–529.CrossRefGoogle Scholar
  26. Fritz, U., Barata, M., Busack, S. D., Fritzsch, G., & Castilho, R. (2006b). Impact of mountain chains, sea straits and peripheral populations on genetic and taxonomic structure of a freshwater turtle, Mauremys leprosa. Zoologica Scripta, 35, 97–108.CrossRefGoogle Scholar
  27. Fritz, U., Guicking, D., Kami, H., Arakelyan, M., Auer, M., Ayaz, D., Ayres Fernández, C., Bakiev, A. G., Celani, A., Džukić, G., Fahd, S., Havaš, P., Joger, U., Khabibullin, V. F., Mazanaeva, L. F., Široký, P., Tripepi, S., Valdeón Vélez, A., Velo Antón, G., & Wink, M. (2007). Mitochondrial phylogeography of European pond turtles (Emys orbicularis, Emys trinacris) – an update. Amphibia-Reptilia, 28, 418–426.CrossRefGoogle Scholar
  28. Fritz, U., Ayaz, D., Hundsdörfer, A. K., Kotenko, T., Guicking, D., Wink, M., Tok, C. V., Çiçek, K., & Buschbom, J. (2009a). Mitochondrial diversity of European pond turtles (Emys orbicularis) in Anatolia and the Ponto-Caspian Region: multiple old refuges, hotspot of extant diversification and critically endangered endemics. Organisms, Diversity and Evolution, 9, 100–114.CrossRefGoogle Scholar
  29. Fritz, U., Harris, D. J., Fahd, S., Rouag, R., Graciá Martínez, E., Giménez Casalduero, A., Široký, P., Kalboussi, M., Jdeidi, T. B., & Hundsdörfer, A. K. (2009b). Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: old complex divergence in North Africa and recent arrival in Europe. Amphibia-Reptilia, 30, 63–80.CrossRefGoogle Scholar
  30. Georgialis, G. L., & Kear, B. P. (2013). The fossil turtles of Greece: an overview of taxonomy and distribution. Geobios, 46, 299–311.CrossRefGoogle Scholar
  31. Giacalone, G., Lo Valvo, M., & Fritz, U. (2009). Phylogeographic link between Sicilian and Corso-Sardinian Testudo h. hermanni confirmed. Acta Herpetologica, 4, 119–123.Google Scholar
  32. Glaubitz, J. C. (2004). convert: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes, 4, 309–310.CrossRefGoogle Scholar
  33. Goudet, J. (1995). fstat (version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86, 485–486.Google Scholar
  34. Graciá, E., Giménez, A., Anadón, J. D., Harris, D. J., Fritz, U., & Botella, F. (2013). The uncertainty of Late Pleistocene range expansions in the western Mediterranean: a case study of the colonization of south-eastern Spain by the spur-thighed tortoise, Testudo graeca. Journal of Biogeography, 40, 323–334.CrossRefGoogle Scholar
  35. Guicking, D., Joger, U., & Wink, M. (2008). Molecular phylogeography of the viperine snake Natrix maura (Serpentes: Colubridae): evidence for strong intraspecific differentiation. Organisms, Diversity and Evolution, 8, 130–145.CrossRefGoogle Scholar
  36. Gustincich, S., Manfioletti, G., del Sal, G., Schneider, C., & Carninci, C. (1991). A fast method for high-quality genomic DNA extraction from whole human blood. BioTechniques, 11, 298–302.PubMedGoogle Scholar
  37. Hall, T. A. (1999). bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  38. Hervet, S. (2000). Tortues du Quaternaire de France: critères de détermination, répartitions chronologique et géographique. Mésogée, 58, 3–47.Google Scholar
  39. Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322–1332.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hutchison, J. H. (1981). Emydoidea (Emydidae, Testudines) from the Barstovian (Miocene) of Nebraska. PaleoBios, 37, 1–6.Google Scholar
  41. ICZN [International Commission on Zoological Nomenclature]. (1999). International Code of Zoological Nomenclature (4th ed.). London: International Trust for Zoological Nomenclature.Google Scholar
  42. Jiménez Fuentes, E. (1980). Los quelonios del sitio de ocupación achelense de Áridos-1 (Arganda, Madrid). In M. Santonja, N. López, & A. Pérez (Eds.), Ocupaciones achelenses en el Valle del Jarama (pp. 139–143). Madrid: Exelentisima Diputación Provincial de Madrid.Google Scholar
  43. Lenk, P., Fritz, U., Joger, U., & Wink, M. (1999). Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Molecular Ecology, 8, 1911–1922.PubMedCrossRefGoogle Scholar
  44. Li, C., Lu, G., & Orti, G. (2008). Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci. Systematic Biology, 57, 519–539.PubMedCrossRefGoogle Scholar
  45. Linnaeus, C. (1758). Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Tomus I. Regnum Animale. Editio Decima, Reformata. Stockholm: Laurentius Salvius.Google Scholar
  46. Loveridge, A., & Williams, E. E. (1957). Revision of the African tortoises and turtles of the suborder Cryptodira. Bulletin of the Museum of Comparative Zoology, 115, 163–557.Google Scholar
  47. McDowell, S. B. (1964). Partition of the genus Clemmys and related problems in the taxonomy of the aquatic Testudinidae. Proceedings of the Zoological Society London, 143, 239–279.CrossRefGoogle Scholar
  48. Moritz, C. (1994). Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology and Evolution, 9, 373–375.PubMedCrossRefGoogle Scholar
  49. Paulo, O. S., Pinheiro, J., Miraldo, A., Bruford, M. W., Jordan, W. C., & Nichols, R. A. (2008). The role of vicariance vs. dispersal in shaping genetic patterns in ocellated lizard species in the western Mediterranean. Molecular Ecology, 17, 1535–1551.PubMedCrossRefGoogle Scholar
  50. Pedall, I., Schäfer, H., Fritz, U., & Wink, M. (2009). Isolation of microsatellite markers in the Emys orbicularis complex and development of multiplex PCR amplification. Conservation Genetics, 10, 725–727.CrossRefGoogle Scholar
  51. Pedall, I., Fritz, U., Stuckas, H., Valdéon, A., & Wink, M. (2011). Gene flow across secondary contact zones of the Emys orbicularis complex in the Western Mediterranean and evidence for extinction and re-introduction of pond turtles on Corsica and Sardinia (Testudines: Emydidae). Journal of Zoological Systematics and Evolutionary Research, 49, 44–57.CrossRefGoogle Scholar
  52. Perez, M., Livoreil, B., Mantovani, S., Boisselier, M.-C., Crestanello, B., Abdelkrim, J., Bonillo, C., Goutner, V., Lambourdière, J., Pierpaoli, M., Sterijovski, B., Tomovic, L., Vilaça, S. T., Mazzotti, S., & Bertorelle, G. (2014). Genetic variation and population structure in the endangered Hermann’s tortoise: the roles of geography and human-mediated processes. Journal of Heredity, 105, 70–81.PubMedCrossRefGoogle Scholar
  53. Pleguezuelos, J. M., Brito, J. C., Fahd, S., Feriche, M., Mateo, J. A., Moreno-Rueda, G., Reques, R., & Santos, X. (2010). Setting conservation priorities for the Moroccan herpetofauna: the utility of regional red listing. Oryx, 14, 501–508.CrossRefGoogle Scholar
  54. Posada, D. (2008). jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.PubMedCrossRefGoogle Scholar
  55. Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.PubMedCentralPubMedGoogle Scholar
  56. Recuero, E., Iraola, A., Rubio, X., Machordom, A., & García-París, M. (2007). Mitochondrial differentiation and biogeography of Hyla meridionalis (Anura: Hylidae): an unusual phylogeographical pattern. Journal of Biogeography, 34, 1207–1219.CrossRefGoogle Scholar
  57. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.Google Scholar
  58. Rosenberg, N. A. (2004). distruct: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138.Google Scholar
  59. Sambrook, J., & Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual (3rd ed.). Cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory Press.Google Scholar
  60. Santos, X., Rato, C., Carranza, S., Carretero, M. A., & Pleguezuelos, J. M. (2012). Complex phylogeography in the southern smooth snake (Coronella girondica) supported by mtDNA sequences. Journal of Zoological Systematics and Evolutionary Research, 50, 210–219.CrossRefGoogle Scholar
  61. Schleich, H. H., Kästle, W., & Kabisch, K. (1996). Amphibians and Reptiles of North Africa. Königstein: Koeltz Scientific Publishers.Google Scholar
  62. Sommer, R. S., Persson, A., Wieseke, N., & Fritz, U. (2007). Holocene recolonization and extinction of the pond turtle, Emys orbicularis (L., 1758), in Europe. Quaternary Science Reviews, 26, 3099–3107.CrossRefGoogle Scholar
  63. Sommer, R. S., Lindqvist, C., Persson, A., Bringsøe, H., Rhodin, A. G. J., Schneeweiss, N., Široký, P., Bachmann, L., & Fritz, U. (2009). Unexpected early extinction of the European pond turtle (Emys orbicularis) in Sweden and climatic impact on its Holocene range. Molecular Ecology, 18, 1252–1262.PubMedCrossRefGoogle Scholar
  64. Spinks, P. Q., & Shaffer, H. B. (2009). Conflicting mitochondrial and nuclear phylogenies for the widely disjunct Emys (Testudines: Emydidae) species complex, and what they tell us about biogeography and hybridization. Systematic Biology, 58, 1–20.PubMedCrossRefGoogle Scholar
  65. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.PubMedCrossRefGoogle Scholar
  66. Stöck, M., Sicilia, A., Belfiore, N. M., Buckley, D., Lo Brutto, S., Lo Valvo, M., & Arculeo, M. (2008). Post-Messinian evolutionary relationships across the Sicilian channel: mitochondrial and nuclear markers link a new green toad from Sicily to African relatives. BMC Evolutionary Biology, 8, 56.PubMedCentralPubMedCrossRefGoogle Scholar
  67. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6. Molecular Biology and Evolution, 30, 2725–2729.PubMedCrossRefGoogle Scholar
  68. van Dijk, P. P., Iverson, J. B., Shaffer, H. B., Bour, R., & Rhodin, A. G. J. (2012). Turtles of the world, 2012 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. In A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, J. B. Iverson, & R. A. Mittermeier (Eds.), Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group (pp. 000.243–000.328). Lunenburg, MA: Chelonian Research Foundation. Chelonian Research Monographs, 5.Google Scholar
  69. Veith, M., Mayer, C., Samraoui, B., Donaire Barroso, D., & Bogaerts, S. (2004). From Europe to Africa and vice versa: evidence for multiple intercontinental dispersal in ribbed salamanders (genus Pleurodeles). Journal of Biogeography, 31, 159–171.CrossRefGoogle Scholar
  70. Velo-Antón, G., Godinho, R., Ayres, C., Ferrand, N., & Cordero Rivera, A. (2007). Assignment tests applied to relocate individuals of unknown origin in a threatened species, the European pond turtle (Emys orbicularis). Amphibia-Reptilia, 28, 475–484.CrossRefGoogle Scholar
  71. Velo-Antón, G., García-París, M., & Cordero Rivera, A. (2008). Patterns of nuclear and mitochondrial DNA variation in Iberian populations of Emys orbicularis (Emydidae): conservation implications. Conservation Genetics, 9, 1263–1274.CrossRefGoogle Scholar
  72. Velo-Antón, G., Wink, M., Schneeweiss, N., & Fritz, U. (2011). Native or not? Tracing the origin of wild-caught and captive freshwater turtles in a threatened and widely distributed species (Emys orbicularis). Conservation Genetics, 12, 583–588.CrossRefGoogle Scholar
  73. Velo-Antón, G., Godinho, R., Harris, D. J., Santos, F., Martínez-Freiria, F., Fahd, S., Larbes, S., Pleguezuelos, J. M., & Brito, J. C. (2012). Deep evolutionary lineages in a Western Mediterranean snake (Vipera latastei/monticola group) and high genetic structuring in Southern Iberian populations. Molecular Phylogenetics and Evolution, 65, 965–973.PubMedCrossRefGoogle Scholar
  74. Wiens, J. J., Kuczynski, C. A., & Stephens, P. R. (2010). Discordant mitochondrial and nuclear gene phylogenies in emydid turtles: implications for speciation and conservation. Biological Journal of the Linnean Society, 99, 445–461.CrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2014

Authors and Affiliations

  • Heiko Stuckas
    • 1
  • Guillermo Velo-Antón
    • 2
  • Soumia Fahd
    • 3
  • Mohsen Kalboussi
    • 4
  • Rachid Rouag
    • 5
  • Marco Arculeo
    • 6
  • Federico Marrone
    • 6
  • Francesco Sacco
    • 6
  • Melita Vamberger
    • 1
  • Uwe Fritz
    • 1
    Email author
  1. 1.Museum of Zoology, Senckenberg DresdenDresdenGermany
  2. 2.CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos GenéticosUniversidade do PortoVairãoPortugal
  3. 3.Département de Biologie, Faculté des SciencesUniversité Abdelmalek EssaâdiTétouanMorocco
  4. 4.Institut Sylvo-PastoralTabarkaTunisia
  5. 5.Institut d’Agronomie, Centre universitaire d’El TarfEl TarfAlgeria
  6. 6.Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche (STEBICEF)Università di PalermoPalermoItaly

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