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Biological Invasions

, Volume 18, Issue 8, pp 2123–2135 | Cite as

Spartina versicolor Fabre: Another case of Spartina trans-Atlantic introduction?

  • A. Baumel
  • M. Rousseau-Gueutin
  • C. Sapienza-Bianchi
  • A. Gareil
  • N. Duong
  • H. Rousseau
  • O. Coriton
  • R. Amirouche
  • S. Sciandrello
  • B. Duarte
  • I. Caçador
  • J. M. Castillo
  • M. Ainouche
Invasive Spartina

Abstract

Intercontinental introductions are widespread in the genus Spartina, with important ecological and evolutionary consequences. The native or introduced status of Spartina species is then critical with regard to biodiversity assessment, especially for vulnerable Mediterranean coastline ecosystems. Spartina versicolor was first recorded in southern France in 1849, then successively in various places on the European and North-African Mediterranean and Atlantic coasts. This species is considered to be either a European native or an invasive species introduced from North America which has a high morphological similarity to the Atlantic American species Spartina patens. We performed extensive sampling of S. versicolor in Europe and North Africa (from natural populations and herbarium collections) and compared these samples to other European and American Spartina species (including S. patens). Chromosome counts were reported for the first time and revealed that S. versicolor is tetraploid (2n = 4x = 40). Phylogenetic analyses based on chloroplast and nuclear ribosomal DNA sequences did not reveal any molecular variation within S. versicolor. In this species, a single haplotype, that is identical to one haplotype of S. patens, was found in the four chloroplast and the nuclear ribosomal ITS regions investigated. In addition, simple sequence repeat markers were used and revealed a low level of genetic diversity within S. versicolor, suggesting that the introduction of S. versicolor occurred from a narrow genetic pool of S. patens from North America.

Keywords

Cordgrass Genetic diversity Species status Mediterranean Microsatellites Phylogeny 

Notes

Acknowledgments

This work was supported by the “Biological Invasion” Programme of UMR-CNRS Ecobio, University of Rennes 1 (France), the IMBE molecular biology service, the International Associated Laboratory LIA ECOGEN and the Partner University Funds (to M. A.). We gratefully acknowledge financial support from the “Région Bretagne” and the European Union Seventh Framework Programme [FP7-CIG-2013–2017; Grant no. 333709 to M. R-G.]. We thank members of herbaria in France (Herbier Montpellier Université, Herbier du Muséum d’Histoire Naturelle de Marseille, Herbier Paris, Université de Rennes 1) for providing access to historical reference samples, and to the many people who helped us getting plant samples from various places (listed in Supplementary table S1), and most particularly: G. Martin, O. Garsmeur, E. Vela, J-M. Lewin, C. Piazza, J. Xiao Wen Wong, (Old World S. versicolor) M-E. Siqueiros, M. Gross and C. Richards (New World S. patens). The authors also thank D. Ayres and one anonymous reviewer for helpful comments on an earlier version of this manuscript.

Supplementary material

10530_2016_1128_MOESM1_ESM.xlsx (18 kb)
Supplementary material 1 (XLSX 18 kb)
10530_2016_1128_MOESM2_ESM.xlsx (44 kb)
Supplementary material 2 (XLSX 44 kb)

References

  1. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173Google Scholar
  2. Ainouche ML, Chelaifa H, Ferreira de Carvalho J, Bellot S, Ainouche AK, Salmon A (2012) Polyploid evolution in Spartina: dealing with highly redundant hybrid genomes. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Berlin, pp 225–243Google Scholar
  3. An SQ, Gu BH, Zhou CF et al (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res 47:183–191CrossRefGoogle Scholar
  4. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrass and hybrids (Spartina sp) in the tidal marshes of San-Francisco Bay CA, USA. Biol Invasions 6:221–231CrossRefGoogle Scholar
  5. Baumel A, Ainouche ML, Levasseur JE (2001) Molecular investigations in populations of Spartina anglica CE Hubbard (Poaceae) invading coastal Brittany (France). Mol Ecol 10:1689–1701CrossRefPubMedGoogle Scholar
  6. Baumel A, Ainouche ML, Bayer RJ, Ainouche AK, Misset MT (2002) Molecular phylogeny of hybridizing species from the genus Spartina Schreb. (Poaceae). Mol Phylogenet Evol 22:303–314CrossRefPubMedGoogle Scholar
  7. Baumel A, Ainouche ML, Misset MT, Gourret JP, Bayer RJ (2003) Genetic evidence for hybridization between the native Spartina maritima and the introduced Spartina alterniflora (Poaceae) in South-West France: Spartina neyrautii re-examined. Plant Syst Evol 237:87–97CrossRefGoogle Scholar
  8. Bertacci A, Lombardi T (2014) Spartina versicolor Fabre in coastal areas of Tuscany (Italy). Contrib Bot XLIX:49–60Google Scholar
  9. Blum MJ, Bando KJ, Katz M (2007) Geographic structure, genetic diversity and source tracking of Spartina alterniflora. J Biogeogr 34:2055–2069CrossRefGoogle Scholar
  10. Bortolus A (2006) The austral cordgrass Spartina densiflora Brong: its taxonomy, biogeography and natural history. J Biogeogr 33:158–168CrossRefGoogle Scholar
  11. Bortolus A, Carlton JT, Schwindt E (2015) Reimagining South American coasts: unveiling the hidden invasion history of an iconic ecological engineer. Divers Distrib 21:1267–1283CrossRefGoogle Scholar
  12. Boutte J, Aliaga B, Lima O, Ferreira de Carvalho J, Ainouche A, Macas J, Rousseau-Gueutin M, Coriton O, Ainouche M, Salmon A (2015) Haplotype detection from next-generation sequencing in high-ploidy-level species: 45S rDNA gene copies in the hexaploid spartina maritima. G3 6:29–40CrossRefPubMedPubMedCentralGoogle Scholar
  13. Burdick DM, Mendelssohn IA (1987) Waterlogging responses in dune, swale, and marsh populations of Spartina patens under field conditions. Oecologia 74:321–329CrossRefGoogle Scholar
  14. Burdick DM, Mendelssohn IA, McKee KL (1989) Live standing crop and metabolism of the salt marsh grass Spartina patens as related to edaphic factors in a brackish, mixed marsh community in Louisiana. Estuaries 12:195–204CrossRefGoogle Scholar
  15. Campos JA, Herrera M, Biurrun I, Loidi J (2004) The role of alien plants in the natural coastal vegetation in central-northern Spain. Biodivers Conserv 13:2275–2293CrossRefGoogle Scholar
  16. Casolo V, Tomasella M, De Col V, Braidot E, Savi T, Nardini A (2014) Water relations of an invasive halophyte (Spartina patens): osmoregulation and ionic effects on xylem hydraulics. Funct Plant Biol 42:264–273Google Scholar
  17. Castillo JM, Mateos-Naranjo E, Nieva FJ, Figueroa E (2008) Plant zonation at salt marshes of the endangered cordgrass Spartina maritima invaded by Spartina densiflora. Hydrobiologia 614:363–371CrossRefGoogle Scholar
  18. Castillo JM, Ayres DR, Leira-Docel P, Bailey J, Blum M, Strong DR, Luque T, Figueroa E (2010) The production of hybrids with high ecological amplitude between exotic Spartina densiflora and native S maritima in the Iberian Peninsula. Divers Distrib 16:547–558CrossRefGoogle Scholar
  19. Chevalier MA (1923) Note sur les Spartina de la flore française. Bull Soc Bot Fr 70:54–63CrossRefGoogle Scholar
  20. Cosson E, Durieu de Maisonneuve (1867) Introduction à la flore d’Algérie. Phanérogamie. Groupe des Glumacées (seu descriptio glumacearum in Algeria nascentium). Exploration Scientifique de l’Algérie, publiée par ordre du Gouvernement. Sciences Naturelles. Botanique. Imprimerie Impériale. ParisGoogle Scholar
  21. Coste H (1906) Flore de la France. T.III. Librairie des Sciences Naturelles, Paris, p 807Google Scholar
  22. Cottet M, De Montaudouin X, Blanchet H, Lebleu P (2007) Spartina anglica eradication experiment and in situ monitoring assess structuting strength of habitat complexity on marine macrofauna at high tidal level. Estuar Coast Shelf S 71:629–640CrossRefGoogle Scholar
  23. Daehler CC, Strong DR (1996a) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Conserv 78:51–58CrossRefGoogle Scholar
  24. Daehler CC, Strong DR (1996b) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Conserv 78:51–58CrossRefGoogle Scholar
  25. Daveau J (1897) La flore littorale du Portugal. Bol Soc Brot 14:4–54Google Scholar
  26. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20CrossRefGoogle Scholar
  27. Drummond AJ, Ashton B, Buxton S et al (2010) Geneious v5.1. http://www.geneious.com
  28. Fabre ME (1849) Description d’une nouvelle espèce de Spartina, abondante sur une portion du littoral méditerranéen. Ann Sci Nat Bot Biol 3:122–125Google Scholar
  29. Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  30. Ferreira de Carvalho J, Chelaifa H, Boutte J et al (2013) Exploring the genome of the salt- marsh Spartina maritima (Poaceae, Chloridoideae) through BAC end sequence analysis. Plant Mol Biol 83:591–606CrossRefPubMedGoogle Scholar
  31. Foote AL, Reynolds KA (1997) Decomposition of saltmeadow cordgrass (Spartina patens) in Louisiana coastal marshes. Estuaries 20:579–588CrossRefGoogle Scholar
  32. Fortune PM, Schierenbeck KA, Ainouche AK, Jacquemin J, Wendel JF et al (2007) Evolutionary dynamics of Waxy and the origin of hexaploid Spartina species (Poaceae). Mol Phylogenet Evol 43:1040–1055CrossRefPubMedGoogle Scholar
  33. Fortune PM, Schierenbeck K, Ayres D, Bortolus A, Clatrice O, Ainouche ML (2008) The enigmatic invasive Spartina densiflora: a history of hybridizations in a polyploidy context. Mol Ecol 17:4304–4316CrossRefPubMedGoogle Scholar
  34. Frasco BA, Good RE (1982) Decomposition dynamics of Spartina alterniflora and Spartina patens in a New Jersey salt marsh. Am J Bot 69:402–406CrossRefGoogle Scholar
  35. Giuliano M, Stanisci A (2010) Biodiversity conservation in coastal areas in molise (Italy). Bol Mus Ist Biol Univ Genova 72:144–147Google Scholar
  36. Gray AJ, Benham PEM, Raybould AF (1990) Spartina anglica—the evolutionary and ecological background. In: Gray AJ, Benham PEM (eds) Spartina anglicaa research review. Institute of Terrestrial Ecology, Natural Environment Research Council, 5–10Google Scholar
  37. Gray AJ, Marshall DF, Raybould AF (1991) A century of evolution in Spartina anglica. Adv Ecol Res 21:1–62CrossRefGoogle Scholar
  38. Guénégou MC, Citharel J, Levasseur JE (1988) The hybrid status of Spartina anglica (Poaceae). Enzymatic analysis of the species and the presumed parents. Can J Bot 66:1830–1833Google Scholar
  39. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704CrossRefPubMedGoogle Scholar
  40. Hacker SD, Heimer D, Hellquist CE, Reeder TG, Reeves B, Riordan TJ Jr, Dethier MN (2001) A marine plant (Spartina anglica) invades widely varying habitats: potential mechanisms of invasion and control. Biol Invasions 3:211–217CrossRefGoogle Scholar
  41. Hardion L, Baumel A, Verlaque R, Vila B (2014) Distinct evolutionary histories of lowland biota on Italian and Balkan peninsulas revealed by the phylogeography of Arundo plinii (Poaceae). J Biogeogr 41:2150–2161CrossRefGoogle Scholar
  42. Hounsome G (2013) Spartina patens in West Sussex. Bot Soc Br Isles BBSI News 123:66–67Google Scholar
  43. Hubbard JCE (1968) Grasses, 2nd edn. Penguin Books, LondonGoogle Scholar
  44. Jaccard P (1901) Distribution de la flore alpine dans le bassin des Dranses et dans quelques régions voisines. Bull Soc Vaud Sci Nat 37:241–272Google Scholar
  45. Jeanmonod D, Burdet HM (1989) Notes et contributions à la flore de Corse IV. Candollea 44:337–401Google Scholar
  46. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  47. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kim S, Rayburn AL, Voigt TB, AinoucheML Ainouche AK, Lee DK (2013) Chloroplast DNA intraspecific phylogeography of Prairie Cordgrass (Spartina pectinata Bosc ex Link). Plant Mol Biol Rep 31:1376–1383CrossRefGoogle Scholar
  49. Kowarik I (2003) Human agency in biological invasions: secondary releases foster naturalisation and population expansion of alien plant species. Biol Invasions 5:293–312Google Scholar
  50. Lonard RI, Judd FW, Stalter R (2010) The biological flora of coastal dunes and wetlands: Spartina patens (W. Aiton) G.H. Muhlenberg. J Coast Res 265:935–946CrossRefGoogle Scholar
  51. Mansion G, Rosenbaum G, Schoenenberger N, Bacchetta G, Rossell’o J, Conti E (2008) Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the mediterranean basin by the angiosperm family Araceae. Syst Biol 57:269–285CrossRefPubMedGoogle Scholar
  52. Marchant CJ (1968) Evolution in Spartina (Gramineae). III. Species chromosome numbers and their taxonomic significance. Bot J Linn Soc 60:41–47Google Scholar
  53. Marignani M, Bacchetta G, Bagella S, Carmela Caria M, Delogu F, Farris E, Fenu G, Filigheddu R, Blasi C (2014) Is time on our side? Strengthening the link between field efforts and conservation needs. Biodivers Conserv 23:421–431CrossRefGoogle Scholar
  54. Médail F, Verlaque R (1997) Ecological characteristics and rarity of endemic plants from southeast France and Corsica: implications for biodiversity conservation. Biol Conserv 80:269–281CrossRefGoogle Scholar
  55. Migliore J, Baumel A, Juin M, Fady B, Roig A, Duong N, Médail F (2013) Surviving in mountain climate refugia: new insights from the genetic diversity and structure of the relict shrub Myrtus nivellei (Myrtaceae) in the Sahara Desert. PLoS One 8:e73795CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mobberley D (1956) Taxonomy and distribution of the genus Spartina. Iowa State Coll J Sci 30:471–574Google Scholar
  57. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  58. Oksanen J, Blanchet FG, Kindt R et al (2013) vegan: community ecology package. R package version 2.0-7. http://CRAN.R-project.org/package=vegan
  59. Page HM, Lastra M, Rodil IF et al (2010) Effects of non-native Spartina patens on plant and sediment organic matter carbon incorporation into the local invertebrate community. Biol Invasions 12:3825–3838CrossRefGoogle Scholar
  60. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  61. Parlatore F (1850) Flora Italiana. I. Tipografia Le Monnier, FirenzeGoogle Scholar
  62. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  63. Peterson PM, Romaschenko K, Herrera Arrieta Y, Saarela JM (2014) A molecular phylogeny and new subgeneric classification of Sporobolus (Poaceae: Chloridoideae: Sporobolinae). Taxon 63:1212–1243CrossRefGoogle Scholar
  64. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefPubMedGoogle Scholar
  65. Prieto JAF, Cires E, Sanchez Corominas T et al (2011) Systematics and management of natural resources: the case of Spartina species on European shores. Biologia 66:1011–1018CrossRefGoogle Scholar
  66. Rousseau-Gueutin M, Bellot S, Martin GE et al (2015) The chloroplast genome of the hexaploid Spartina maritima (Poaceae, Chloridoideae): comparative analyses and molecular dating. Mol Phylogenet Evol 93:5–16CrossRefPubMedGoogle Scholar
  67. Saarela JM (2012) Taxonomic synopsis of invasive and native Spartina (Poaceae, Chloridoideae) in the Pacific Northwest (British Columbia, Washington and Oregon), including the first report of Spartina x townsendii for British Columbia, Canada. PhytoKeys 10:25–82Google Scholar
  68. Saint-Yves A (1932) Monographia spartinum. Candollea 5:19–100Google Scholar
  69. Sanchéz-Gullón E (2001) Spartina versicolor (Poaceae): novedad agrotológica para Andalucía. Acta Liotan Malacit 26:279–280Google Scholar
  70. SanLeón DG, Izco J, Sánchez JM (1999) Spartina patens as a weed in Galician saltmarshes (NW Iberian Peninsula). Hydrobiologia 415:213–222CrossRefGoogle Scholar
  71. Sanz Elorza M, Dana Sánchez ED, Sobrino Vesperinas E (2004) Atlas de las plantas alóctonas invasoras en España. Dirección General para la Biodiversidad, Madrid, p 384Google Scholar
  72. Silander JA (1984) The genetic basis of the ecological amplitude of Spartina patens. III. Allozyme variation. Bot Gaz 569–577Google Scholar
  73. Silander J, Antonovics J (1979) The genetic basis of the ecological amplitude of Spartina patens. Morphometric and physiological traits. Evolution 33:1114–1127CrossRefGoogle Scholar
  74. Stace C (2010) New flora of the British Isles. Cambridge University Press, CambridgeGoogle Scholar
  75. Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Ann Rev Ecol Evol Syst 44:389–410CrossRefGoogle Scholar
  76. Swofford DL (2001) Phylogenetic analysis using Parsimony (* and other methods). Version 4.0. Sinauer Associates. Sunderland, MassachusettsGoogle Scholar
  77. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109Google Scholar
  78. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  79. Tison JM, de Foucault B (2014) Flora gallica. Flore de France, Biotope, MèzeGoogle Scholar
  80. Tison JM, Jauzein P, Michaud H (2014) Flore de la France Mediterranéenne Continentale. Naturalia, PorquerollesGoogle Scholar
  81. Valsecchi F (1962) Spartina juncea Willd. nuova specie per la Sardegna. Giorn Bot Italy 69:3–47Google Scholar
  82. Valtuena FJ, Preston CD, Kadereit JW (2011) Evolutionary significance of the invasion of introduced populations into the native range of Meconopsis cambrica. Mol Ecol 20:4318–4331CrossRefPubMedGoogle Scholar
  83. Verlaque R, Aboucaya A, Fridlender A (2002) Les xénophytes envahissants en France: écologie, types biologiques et polyploïdie. Bot Helv 112:121–136Google Scholar
  84. White TJ, Bruns T, Lee S et al (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  85. Wu T (2012) Genetic diversity in Spartina patens in remnant patches in the New Jersey Meadowlands. Master thesis. Rutgers University, New Jersey (USA). http://dx.doi.org/doi:10.7282/T39K498K

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • A. Baumel
    • 1
  • M. Rousseau-Gueutin
    • 2
    • 3
  • C. Sapienza-Bianchi
    • 2
  • A. Gareil
    • 2
  • N. Duong
    • 1
  • H. Rousseau
    • 2
  • O. Coriton
    • 4
  • R. Amirouche
    • 5
  • S. Sciandrello
    • 6
  • B. Duarte
    • 7
  • I. Caçador
    • 7
  • J. M. Castillo
    • 8
  • M. Ainouche
    • 2
  1. 1.Aix Marseille Université, Institut Méditerranéen de Biodiversité et d’Ecologie (IMBE, UMR CNRS, IRD, Avignon Université)Technopôle de l’Environnement Arbois-MéditerranéeAix-en-Provence Cedex 04France
  2. 2.UMR CNRS 6553 Ecobio, OSUR (Observatoire des Sciences de l’Univers de Rennes)Université de Rennes 1/Université Européenne de BretagneRennesFrance
  3. 3.INRA, UMR 1349Institut de Génétique, Environnement et Protection des PlantesLe Rheu CedexFrance
  4. 4.Plate-Forme de Cytogénétique Moléculaire, INRA, UMR 1349Institut de Génétique, Environnement et Protection des PlantesLe Rheu CedexFrance
  5. 5.Université des Sciences et de la Technologie Houari BoumedieneLaboratoire de Biologie et Physiologie des OrganismesBab-EzzouarAlgeria
  6. 6.Department of Biological, Geological and Environmental SciencesUniversity of CataniaCataniaItaly
  7. 7.MARE – Marine and Environmental Sciences CentreFaculty of Sciences of the University of LisbonLisbonPortugal
  8. 8.Departamento de Biología Vegetal y Ecología, Facultad de BiologiaUniversidad de SevillaSevilleSpain

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