History vs. legend: Retracing invasion and spread of Oxalis pes-caprae L. in Europe and the Mediterranean area

Oxalis pes-caprae L. is a South African geophyte that behaves as an invasive in the eurimediterranean area. According to a long-established hypothesis, O. pes-caprae may have invaded Europe and the Mediterranean area starting from a single plant introduced in the Botanical Garden of Malta at the beginning of the 19th century. The aim of this work was to test this hypothesis, to track the arrival of O. pes-caprae in different countries of the Euro-Mediterranean area and to understand the pathways of spreading and particularly its starting point(s). Historical data attesting the presence of the plant in the whole Euro-Mediterranean region were collected from different sources: herbarium specimens, Floras and other botanical papers, plant lists of gardens, catalogs of plant nurseries and plant dealers. First records of the plant (both cultivated and wild) for each Territorial Unit (3rd level of NUTS) were selected and used to draw up a diachronic map and an animated graphic. Both documents clearly show that oldest records are scattered throughout the whole area, proving that the plant arrived in Europe and in the Mediterranean region more times independently and that its spreading started in different times from several different centers of invasion. Botanical gardens and other public or private gardens, nurseries and plant dealers, and above all seaside towns and harbors seemingly played a strategic role as a source of either intentional and unintentional introduction or spread. A geographic profiling analysis was performed to analyse the data. We used also techniques (Silhouette, Kmeans and Voronoi tessellation) capable of verifying the presence of more than one independent clusters of data on the basis of their geographical distribution. Microsatellites were employed for a preliminary analysis of genetic variation in the Mediterranean. Even if the sampling was insufficient, particularly among the populations of the original area, our data supported three main groups of populations, one of them corresponding to the central group of populations identified by GP analysis, and the other two corresponding, respectively, to the western and the eastern cluster of data. The most probable areas of origin of the invasion in the three clusters of observations are characterized by the presence of localities where the invasive plant was cultivated, with the exception of the Iberian cluster of observation where the observations in the field predate the data about known cultivation localities. Alternative possible reasons are also suggested, to explain the current prevalence of pentaploid short-styled plants in the Euro-Mediterranean area.

[1]  Ernest David Marquand Flora of Guernsey and the Lesser Channel Islands: Namely, Alderney, Sark, Herm, Jethou, and the Adjacent Islets , 2015 .

[2]  Alessio Papini,et al.  Methods for geographic profiling of biological invasions with multiple origin sites , 2016, International Journal of Environmental Science and Technology.

[3]  Alessio Papini,et al.  Snow's case revisited: new tool in geographic profiling of epidemiology , 2016, The Brazilian journal of infectious diseases : an official publication of the Brazilian Society of Infectious Diseases.

[4]  R. Piredda,et al.  Application of plastid and nuclear markers to DNA barcoding of Euro-Mediterranean oaks (Quercus, Fagaceae): problems, prospects and phylogenetic implications , 2013 .

[5]  F. Garbari,et al.  Flora esotica d'Italia , 1974 .

[6]  J. Suda,et al.  Variation in DNA-ploidy Levels of Reynoutria Taxa in the Czech Republic. , 2003, Annals of botany.

[7]  L. Navarro,et al.  Invasion Fosters Change: Independent Evolutionary Shifts in Reproductive Traits after Oxalis pes-caprae L. Introduction , 2016, Front. Plant Sci..

[8]  J. Suda,et al.  DNA ploidy‐level variation in native and invasive populations of Lythrum salicaria at a large geographical scale , 2007 .

[9]  Augustin Pyramus de Candolle Catalogus Plantarum Horti Botanici Monspeliensis: Addito Observationum Circa Species Novas Aut Non Satis Cognitas Fasciculo , 2008 .

[10]  Mark D. Stevenson,et al.  Spatial targeting of infectious disease control: identifying multiple, unknown sources , 2014 .

[11]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[12]  B. Foggi,et al.  Karyological investigations on the South African invasive Oxalis pes-caprae L. (Oxalidaceae) in native and invaded areas, with special focus on Italy , 2013 .

[13]  Anil K. Jain Data clustering: 50 years beyond K-means , 2008, Pattern Recognit. Lett..

[14]  D. Kim Rossmo,et al.  Geographic profiling as a novel spatial tool for targeting the control of invasive species , 2012 .

[15]  C. Lavoie,et al.  Reconstructing the spread of invasive plants: taking into account biases associated with herbarium specimens , 2003 .

[16]  L. Navarro,et al.  Sexual reproduction of the pentaploid, short-styled Oxalis pes-caprae allows the production of viable offspring. , 2014, Plant biology.

[17]  R. Hufbauer,et al.  Multiple introductions of two invasive Centaurea taxa inferred from cpDNA haplotypes , 2007 .

[18]  L. Navarro,et al.  Invasion genetics of the Bermuda buttercup (Oxalis pes‐caprae): complex intercontinental patterns of genetic diversity, polyploidy and heterostyly characterize both native and introduced populations , 2015, Molecular ecology.

[19]  L. Viegi,et al.  Contributo alla conoscenza della Flora esotica d’Italia: le specie presenti nelle Marche , 2004 .

[20]  R. Billeter,et al.  Why only tetraploid Solidago gigantea (Asteraceae) became invasive: a common garden comparison of ploidy levels , 2010, Oecologia.

[21]  Alessio Papini,et al.  Tracking the origin of the invading Caulerpa (Caulerpales, Chlorophyta) with Geographic Profiling, a criminological technique for a killer alga , 2012, Biological Invasions.

[22]  Daoyuan Zhang,et al.  Invasion of Lepidium draba (Brassicaceae) in the western United States: distributions and origins of chloroplast DNA haplotypes , 2005, Molecular ecology.

[23]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[24]  G. Anfora,et al.  Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe , 2014, Journal of Pest Science.

[25]  Kazunori Ohno,et al.  Applying geographic profiling used in the field of criminology for predicting the nest locations of bumble bees. , 2010, Journal of theoretical biology.

[26]  J. Lange Pugillus plantarum imprimis Hispanicarum, quas in itinere 1851-52 legit Joh. Lange, 1-4. , 1860 .

[27]  Cytogeography of Oxalis pes-caprae in its native range: where are the pentaploids? , 2013, Biological Invasions.

[28]  L. Navarro,et al.  Variation in the incompatibility reactions in tristylous Oxalis pes-caprae: large-scale screening in South African native and Mediterranean basin invasive populations , 2017 .

[29]  R. Gardner,et al.  A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. , 1999, Genome.

[30]  Roland Brandl,et al.  Weed invasion in East Africa: insights from herbarium records , 1998 .

[31]  Stefano Sommier,et al.  Flora melitensis nova , 1915 .

[32]  Carsten Rahbek,et al.  The patterns and causes of elevational diversity gradients , 2012 .

[33]  Jonathan F Wendel,et al.  Polyploidy and Genome Evolution in Plants This Review Comes from a Themed Issue on Genome Studies and Molecular Genetics Edited , 2022 .

[34]  R. Calamassi,et al.  Stigma and style anatomy and ultrastructure in Italian Oxalis pes-caprae L. and their possible connection with self-incompatibility , 2014 .

[35]  W. G. Spaulding,et al.  Ploidy race distributions since the Last Glacial Maximum in the North American desert shrub, Larrea tridentata , 2002 .

[36]  Conceição Santos,et al.  Distribution of flower morphs, ploidy level and sexual reproduction of the invasive weed Oxalis pes-caprae in the western area of the Mediterranean region. , 2007, Annals of botany.

[37]  R. Nègre Petite flore des régions arides du Maroc occidental , 1961 .

[38]  M. Feldman,et al.  The Impact of Polyploidy on Grass Genome Evolution , 2002, Plant Physiology.

[39]  Reproductive strategy of the invasive Oxalis pes-caprae: distribution patterns of floral morphs, ploidy levels and sexual reproduction , 2013, Biological Invasions.

[40]  C. Robin,et al.  A next-generation sequencing method for overcoming the multiple gene copy problem in polyploid phylogenetics, applied to Poa grasses , 2011, BMC Biology.

[41]  H. G. Baker,et al.  Characteristics and modes of origin of weeds. , 1965 .

[42]  R. Ornduff Reproductive systems and chromosome races of Oxalis pes-caprae L. and their bearing on the genesis of a noxious weed , 1987 .

[43]  P. Pyšek,et al.  Invasion history of Oenothera congeners in Europe: a comparative study of spreading rates in the last 200 years , 2001 .

[44]  R. Piredda,et al.  Plastome data reveal multiple geographic origins of Quercus Group Ilex , 2016, PeerJ.

[45]  Miguel Colmeiro y Penido,et al.  Enumeración y revisión de las plantas de la Peninsula Hispano-Lusitana é Islas Baleares, , 1885 .