[en] The last century has seen an unparalleled movement of species around the planet as a direct result of human activity, which has been a major contributor to the biodiversity crisis. Amphibians represent a particularly vulnerable group, exacerbated by the devastating effects of chytrid fungi. We report the malicious translocation and establishment of the alpine newt (Ichthyosaura alpestris) to its virtual antipode in North Island of New Zealand. We use network analysis of mitochondrial DNA haplotypes to identify the original source population as I. a. apuana from Tuscany, Italy. Additionally, a population in southern France, presumed to be introduced, is identified as I. a. alpestris from western Europe. However, the presence of two differentiated haplotypes suggests a mixed origin. This type of analysis is made possible by the recent availability of a phylogenetic analysis of the species throughout its natural range. We discuss the particulars of both introductions.
Disciplines :
Life sciences: Multidisciplinary, general & others Genetics & genetic processes Aquatic sciences & oceanology
Author, co-author :
Arntzen, Jan W.; Naturalis Biodiversity Center, The Netherlands
King, Tania M.; University of Otago, New Zealand > Department of Zoology
Denoël, Mathieu ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Martínez-Solano, Iñigo; Universidade do Porto > CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos,
Wallis, Graham P.; University of Otago > Department of Zoology
Language :
English
Title :
Provenance of Ichthyosaura alpestris (Caudata: Salamandridae) introductions to France and New Zealand assessed by mitochondrial DNA analysis
Publication date :
January 2016
Journal title :
Herpetological Journal
ISSN :
0268-0130
Publisher :
British Herpetological Society, United Kingdom
Volume :
26
Issue :
1
Pages :
49-56
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique ULg FSR - Université de Liège. Fonds spéciaux pour la recherche
Aagaard, K. & Lockwood, J. (2014). Exotic birds show lags in population growth. Diversity and Distributions 20, 547-554.
Allen, R.B. & Lee, W.G., eds. (2006). Biological Invasions in New Zealand. Berlin: Springer.
Arano, B., Arntzen, J.W., Herrero, P. & García-París, M. (1991). Genetic differentiation among Iberian populations of the Alpine newt, Triturus alpestris. Amphibia-Reptilia 21, 409-421.
Arévalo, E., Davis, S.K. & Sites, J.W. (1994). Mitochondrial-DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Systematic Biology 43, 387-418.
Arntzen, J.W., Burke, T. & Jehle, R. (2010). Estimating the propagule size of a cryptogenic crested newt population. Animal Conservation 13, 74-81.
Arntzen, J.W., Denoël, M., Kuzmin, S., Ishchenko, V., et al. (2009). Mesotriton alpestris. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Available from: . Accessed: 05 June 2014.
Arntzen, J.W. & Thorpe, R.S. (1999). Italian Crested newts in the Basin of Geneva: distribution and genetic interactions with autochtonous species. Herpetologica 55, 423-433.
Bell, B.D. & Bell, A.P. (1995). Distribution of the introduced alpine newt Triturus alpestris and of native Triturus species in north Shropshire, England. Australian Journal of Ecology 20, 367-375.
Bell, B.D. (2010). The threatened leiopelmatid frogs of New Zealand: natural history integrates with conservation. Herpetological Conservation and Biology 5, 515-528.
Bosch, J. & Martínez-Solano, I. (2003). Factors influencing occupancy of breeding ponds in a montane amphibian assemblage. Journal of Herpetology 37, 410-413.
Brede, E.G., Thorpe, R.S., Arntzen, J.W. & Langton, T.E.S. (2000). A morphometric study of a hybrid newt population (Triturus cristatus/T. carnifex): Beam Brook Nurseries, Surrey, U.K. Biological Journal of the Linnean Society 70, 685-695.
Breuil, M. & Parent, G.-H. (1987). Essai de caractérisation du Triton alpestre hellénique Triturus alpestris veluchiensis. 1. Historique et présentation de nouvelles données. Alytes 6, 131-151.
Burdick, A. (2006). Out of Eden. An Odyssey of EcologicalInvasion. New York: Farrar, Strauss & Giroux.
Casquet, J., Thebaud, C. & Gillespie, R.G. (2012). Chelex without boiling, a rapid and easy technique to obtain stable amplifiable DNA from small amounts of ethanol-stored spiders. Molecular Ecology Resources 12, 136-141.
Crooks, J.A. & Soulé, M.E. (1999). Lag times in population explosions of invasive species: causes and implications. Pp. 103-125 in: Invasive species and biodiversity management; Sandlund, O.T., Schei, P.J. & Viken, Å. (eds). Population and Community Biology Series Volume 24. Dordrecht, Kluwer Academic Publishers.
Darriba, D., Taboada, G.L., Doallo, R. & Posada D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
Denoël, M. (1996). Étude comparée du comportement de cour de Triturus alpestris alpestris (Laurenti, 1768) et Triturus alpestris cyreni (Wolterstorff, 1932) (Amphibia, Caudata): approche évolutive. Cahiers d’Ethologie 16, 133-258.
Denoël, M. (2005). Persistance et dispersion d’une population introduite de Triton alpestre (Triturus alpestris) dans les Causses du Larzac (sud de la France). Revue d’Écologie 60, 139-148.
Denoël, M. & Ficetola, G.F. (2008). Conservation of newt guilds in an agricultural landscape of Belgium: the importance of aquatic and terrestrial habitats. Aquatic Conservation: Marine and Freshwater Ecosystems 18, 714-728.
Denoël, M. & Ficetola, G.F. (2014). Heterochrony in a complex world: Disentangling environmental processes of facultative paedomorphosis in an amphibian. Journal of Animal Ecology 83, 606-615.
Denoël, M. & Ficetola, G.F. (2015). Using kernels and ecological niche modelling to delineate conservation areas in an endangered patch-breeding phenotype. Ecological Applications 25, 1922-1931.
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969-1973.
Easteal, S. (1981). The history of introductions of Bufo marinus (Amphibia, Anura): a natural experiment in evolution. Biological Journal of the Linnean Society 16, 93-113.
Elton, C.S. (2000). The Ecology of Invasions by Animals and Plants, Chicago: University of Chicago Press.
Ferracin, A., Lunadei, M. & Falcone, N. (1980). An ecological note on Triturus alpestris apuanus (Bonaparte) and Triturus cristatus carnifex (Laurenti) in the Garfagnana (Lucca, Central Italy). Bolletino di Zoologia 47, 143-147.
Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., et al. (2011). Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194.
Fontelles, F., Guixé, D., Martínez-Silvestre, A., Soler, J. & Villero, D. (2011). Hallada una población introducida de Ommatotriton ophryticus en el Prepirineo catalán. Boletín de la Asociación Herpetológica Española 22, 153-156.
Gabrion, J., Sentein, P. & Gabrion, C. (1977). Les populations néoténiques de Triturus helveticus des Causses et du Bas-Languedoc. I. Répartition et caractéristiques. La Terre et la Vie 31, 489-506.
García-París, M., Martín, C., Dorda, J. & Esteban, M. (1989). Los Anfibios y Reptiles de Madrid. Madrid: Servicio de Extensión Agraria, Ministerio de Agricultura, Pesca y Alimentación.
Geniez, P. & Cheylan, M. (2012). Les Amphibiens et les Reptiles du Languedoc-Roussillon et Régions Limitrophes. Atlas Biogéographique. Mèze & Paris: Biotope & Museum National d’Histoire Naturelle.
Herbert, S.M., Leung, T.L.F. & Bishop, P.J. (2011). Fluorescent probes as a tool for labelling and tracking the amphibian chytrid fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 96, 169-174.
Kats, L.B. & Ferrer, R.P. (2003). Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Diversity and Distributions 9, 99-110.
King, C.M. (1985). Immigrant Killers: Introduced Predators and the Conservation of Birds in New Zealand. Auckland: Oxford University Press.
Kraus, F. (2009). Alien Reptiles and Amphibians: A Scientific Compendium and Analysis. New York: Springer.
Kuzmin, S.L. (1994). Commercial collecting as a threat for amphibian and reptile species of the former Soviet Union. Species 23, 47-48.
Leigh, J.W. & Bryant, D. (2015). popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110-1116
Lever, C. (2003). Naturalized Reptiles and Amphibians of the World. Oxford: Oxford University Press.
Lope, M.J. & Cuadrado, J.A. (1985). Nota sobre la presencia detritón alpino (Triturus alpestris) en el centro de la Península Ibérica. Doñana, Acta Vertebrata 12, 317-318.
Lužnik, M., Varljen Bužan, E. & Kryštufek, B. (2011). Mitochondrial sequences do not support the independent taxonomic position of the extinct Alpine newt subspecies Mesotriton alpestris lacusnigri. Amphibia-Reptilia 32, 435-440.
Martel, A., Blooi, M., Adriaensen, C., van Rooij, P., et al. (2014). Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346, 630-631.
Martel, A., Spitzen-van der Sluijs, A., Blooi, M., Bert, W., et al. (2013). Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences U.S.A. 110, 15325-15329.
Martínez-Solano, I., García-París, M. & Bosch, J. (2006). Anfibios de Peñalara: Identificación y Conservación. Madrid: Dirección General de Promoción y Disciplina Ambiental, Comunidad de Madrid.
Martínez-Solano, I., Bosch, J. & García-París, M. (2003). Demographic trends and community stability in a montane amphibian assemblage. Conservation Biology 17, 238-244.
McDowall, R.M. (1994). Gamekeepers for the Nation: The Story of New Zealand’s Acclimatisation Societies 1861-1990. Christchurch: Canterbury University Press.
McDowall, R.M. (2011). Ikawai: Freshwater Fishes in Maori Culture and Economy. Christchurch: Canterbury University Press.
Measey, G.J., Rödder, D., Green, S.L., Kobayashi, R., et al. (2012). Ongoing invasions of the African clawed frog, Xenopus laevis: a global review. Biological Invasions 14, 2255-2270.
Meilink, W.R.M., Arntzen, J.W., van Delft J.J.C.W. & Wielstra, B. (2015). Genetic pollution of a threatened native crested newt species through hybridization with an invasive congener in the Netherlands. Biological Conservation 184, 145-153.
Mertens, R. & Müller, L. (1928). Liste der Amphibien und Reptilien Europas. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 41, 1-62.
Moreno, V., Aguayo, C.A. & Brunton, D.H. (2011). A survey for the amphibian chytrid fungus Batrachochytrium dendrobatidis in New Zealand’s endemic Hochstetter’s frog (Leiopelma hochstetteri). New Zealand Journal of Zoology 38, 181-184.
Newman, D.G., Bell, B.D., Bishop, P.J., Burns, R., et al. (2010). Conservation status of New Zealand frogs, 2009. New Zealand Journal of Zoology 37, 121-130.
Ohmer, M.E., Herbert, S.M., Speare, R. & Bishop, P.J. (2013). Experimental exposure indicates the amphibian chytrid pathogen poses low risk to New Zealand’s threatened endemic frogs. Animal Conservation 16, 422-429.
Parkes, J. & Murphy, E. (2003). Management of introduced mammals in New Zealand. New Zealand Journal of Zoology 30, 335-359.
Pitt, W., Vice, D. & Pitzler, M. (2005). Challenges of invasive reptiles and amphibians. Proceedings of the Wildlife Damage Management Conference 11, 112-119.
Price, S.J., Garner, T.W.J., Nichols, R.A., Balloux, F., et al. (2014). Collapse of amphibian communities due to an introduced ranavirus. Current Biology 24, 2586-2591.
Pysek, P. & Richardson, D.M. (2010). Invasive species, environmental change and management, and health. Annual Review of Environment and Resources 35, 25-55.
Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014). Tracer v1.6, Available from: .
Rebelo, R., Amaral, P., Bernardes, M., Oliveira, J., et al. (2010). Xenopus laevis (Daudin, 1802), a new exotic amphibian in Portugal. Biological Invasions 12, 3383-3387.
Recuero, E., Buckley, D., García-París, M., Arntzen, J.W., et al. (2014). Evolutionary history of Ichthyosaura alpestris (Caudata, Salamandridae) inferred from the combined analysis of nuclear and mitochondrial markers. Molecular Phylogenetics and Evolution 81, 207-220.
Sentein, P. (1966). L’action du dioxyde de sélénium sur des oeufs d’amphibiens d’espèces résistantes. Chromosoma 19, 357-398.
Sentein, P. (1970). Action de la quinoline sur les mitoses de segmentation des oeufs d’urodèles: le blocage de la centrosphère. Chromosoma 32, 97-134.
Shaw, S.D., Skerratt, L.F., Haigh, A., Bell, B.D., et al. (2013). The distribution and host range of Batrachochytrium dendrobatidis in New Zealand, 1930-2010. Ecology 94, 2108-2111.
Sillero, N., Campos, J., Bonardi, A., Corti, C., et al. (2014). Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia-Reptilia 35, 1-31.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., et al. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651-701.
Sotiropoulos, K., Eleftherakos, K., Džukić, G., Kalezić, M., et al. (2007a). Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Molecular Phylogenetics and Evolution 45, 211-226.
Sotiropoulos, K., Eleftherakos, K., Kalezić, M., Legakis, A. & Polymeni, R. (2007b). Genetic structure of the alpine newt, Mesotriton alpestris (Salamandridae, Caudata), in the southern limit of its distribution: Implications for conservation. Biochemical Systematics and Ecology 36, 297-311.
Spitzen-van der Sluijs, A., Martel, A., Hallmann, C.A., Bosman, W., et al. (2014). Environmental determinants of recent endemism of Batrachochytrium dendrobatidis infections in amphibian assemblages in the absence of disease outbreaks. Conservation Biology 28, 1302-1311.
Tingley, R., Weeks, A.R., Smart, A.S., van Rooyen, A.R., et al. (2015). European newts establish in Australia, marking the arrival of a new amphibian order. Biological Invasions 17, 31-37.
van Delft, J.J.C.W. (2009). Alpenwatersalamander. Mesotriton alpestris. Pp. 96-104 in De Amfibieën en Reptielen van Nederland, De Nederlandse Fauna 9. Creemers, R.C.M. & van Delft, J.J.C.W. (eds). Leiden, Nationaal Natuurhistorisch Museum Naturalis and European Invertebrate Survey.
Villesen, P. (2007). FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes 7, 965-968.
Vitousek, P.M., Mooney, H.A., Lubchenco, J. & Melillo, J.M. (1997). Human domination of Earth’s ecosystems. Science 277, 494-499.
Waldman B., de Wolfshaar, K.V., Andjic, V., Klena, J., et al. (2001). Chytridiomycosis and frog mortality in New Zealand. New Zealand Journal of Zoology 28, 372.