Tracking the Expanding Distribution of Solidago ×Niederederi (Asteraceae) in Europe and First Records from Three Countries Within the Carpathian Region

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BioInvasions Records (2020) Volume 9, Issue 4: 670–684

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Research Article Tracking the expanding distribution of Solidago ×niederederi (Asteraceae) in Europe and first records from three countries within the Carpathian region

Katarína Skokanová1, Barbora Šingliarová1,*, Stanislav Španiel1,2, Iva Hodálová1 and Pavol Mereďa Jr.1 1Institute of Botany, Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 23 Bratislava, Slovakia 2Department of Botany, Faculty of Science, Charles University, Benátská 2, CZ-128 01 Prague, Czechia Author e-mails: [email protected] (KS), [email protected] (BŠ), [email protected] (SŠ), [email protected] (IH), [email protected] (PM) *Corresponding author

Citation: Skokanová K, Šingliarová B, Španiel S, Hodálová I, Mereďa Jr. P (2020) Abstract Tracking the expanding distribution of Solidago ×niederederi (Asteraceae) in Besides the well-known negative effects of invasive plant species on autochthonous Europe and first records from three plant communities, the breakdown of genetic integrity of indigenous species via countries within the Carpathian region. alien-to-native hybridisation represents an additional direct threat to native flora BioInvasions Records 9(4): 670–684, which should not be underestimated. Our aim was to survey the current distribution of https://doi.org/10.3391/bir.2020.9.4.02 Solidago ×niederederi, a hybrid that has originated through spontaneous hybridisation Received: 29 May 2020 between the native European S. virgaurea and allochthonous (North American) Accepted: 24 August 2020 S. canadensis. Although this hybrid was first recorded at the very end of the 19th Published: 20 October 2020 century, most occurrences have been reported during the last decades. It is only known Handling editor: Desika Moodley to grow in Europe and its current distribution is still not well explored. Based on Thematic editor: Stelios Katsanevakis field research in the Carpathians, we list five new localities of S. ×niederederi, which represent the first records of this hybrid in Slovakia, Hungary, and Romania. Copyright: © Skokanová et al. The present paper documents existing reports from 409 sites in 17 European countries. This is an open access article distributed under terms of the Creative Commons Attribution License We provide a detailed list of all records from the literature, freely available databases (Attribution 4.0 International - CC BY 4.0). and webpages as well as a summary map of S. ×niederederi’s known distribution. OPEN ACCESS. In addition, records are analysed regarding a time context and habitat preferences. Finally, we discuss a potential threat that the hybrid could pose to the genetic integrity of the native European populations of the Solidago virgaurea complex.

Key words: plant invasion, hybrid, Solidago canadensis, new chorological records, range expansion

Introduction The worldwide distributed genus Solidago L. includes 120–133 species. North America, with the occurrence of roughly 150 Solidago species and infraspecific taxa, is considered to be the centre of genus diversity (Nesom 2000; Semple and Cook 2006; Semple 2020). The genus is divided into two sections, S. sect. Solidago and S. sect. Ptarmicoidei (House) Semple & Gandhi. The first section is taxonomically complex, rich in species and further subdivided into eleven subsections and one nothosubsection, while S. sect. Ptarmicoidei includes only 7 species and is not further subdivided (Semple and Cook 2006; Gudžinskas and Žalneravičius 2016; Semple 2020). In Europe, only S. sect. Solidago is represented in nature by the

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 670 Expanding distribution of Solidago ×niederederi in Europe

native S. virgaurea complex (from S. subsect. Solidago) and three alien species, S. altissima L. with very restricted distribution (Verloove et al. 2017) and relatively widespread S. canadensis L. and S. gigantea Aiton [all three from S. subsect. Triplinervae (Torr. & A.Gray) G.L. Nesom] (Weber 1998; Kabuce and Priede 2010). In addition, two spontaneous hybrids of native S. virgaurea L. s.s. and alien Solidago species originated in Europe: S. ×niederederi Khek (S. canadensis × S. virgaurea s.s.) and S. ×snarskisii Gudžinskas & Žalneravičius (S. gigantea × S. virgaurea s.s.), both from S. nothosubsect. Triplidago Gudžinskas & Žalneravičius. While to date, S. ×snarskisii is known only from several localities in northern and eastern Europe (Gudžinskas and Žalneravičius 2016; Pliszko 2018; Vinogradova and Galkina 2019), the number of records of S. ×niederederi has rapidly increased over the last decades and has drawn the growing attention of botanists to its (actual and potential) expansion (cf. Jaźwa et al. 2018; Pliszko et al. 2019). Solidago canadensis (2n = 2x = 18) naturally occurs in the north-eastern part of the United States and the southern regions of eastern Canada. Two varieties, S. canadensis var. canadensis and S. canadensis var. hargeri Fernald, are recognised in the native area. They mainly differ in the type of stem indumentum, comprising partly overlapping distributions and weak reproductive isolation (Melville and Morton 1982; Semple and Cook 2006; Semple et al. 2013, 2015). Solidago canadensis is one of the first ornamental plants imported from North America to Europe; it has been introduced to England as early as in 1645 (Kowarik 2003). As an attractive and easy to grow species, it was quickly spread to botanical gardens as well as common gardens and nurseries throughout Europe. In the wild, it was recorded for the first time in 1850 and an exponential increase in the number of its sites in nature began in the years 1870–1900 (Weber 1998). Today, this species is naturalised and invasive in almost all of Europe from northern Italy to southern Scandinavia (Kabuce and Priede 2010). The infraspecific classification of invasive European populations of S. canadensis is still not settled. They have been classified as S. canadensis var. canadensis (e.g. Semple and Cook 2006), or S. canadensis var. hargeri (e.g. Cheek and Semple 2016; Semple 2020), or both varieties had been reported from the continent (e.g. Verloove et al. 2017). Besides Europe, a secondary occurrence of S. canadensis is also known from Asia, Australia, and New Zealand (Semple 2020). Solidago virgaurea (2n = 2x = 18) is a highly polymorphic complex that comprises 14‒24 subspecies and microspecies. The complex is widespread in areas with temperate and cold climates in Europe and Asia and has a patchy distribution in the Mediterranean region of southern Europe, the north- western part of Africa and Asia Minor (Yuzepchuk 1959; Slavík 2004; Greuter 2006‒2020; Sakaguchi et al. 2018; Semple 2020; Semple et al. 2020).

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 671 Expanding distribution of Solidago ×niederederi in Europe

The hybrid S. ×niederederi, a result of homoploid crossing (i.e. at the same ploidy level) of S. canadensis and S. virgaurea s.s., was discovered at the end of the 19th century (see Skokanová et al. 2020). It was defined by authors of its description as “so marvellous that it cannot deny its parental species” (E. Khek in litt., PRC herbarium). The clearly intermediate morphology of S. ×niederederi, in comparison with parental species, was recently documented also by multivariate analyses of morphological traits, especially the height of the plant, size of the synflorescence and capitulum (Karpavičienė and Radušienė 2016). Due to its intermediate morphology, the hybrid plants are relatively easily recognisable in nature during anthesis (e.g., Nilsson 1976; Gudžinskas and Petrulaitis 2016; Pagitz 2016). Besides these traits, plants of S. ×niederederi are, in contrast to the parental species, conspicuous by the frequent presence of vegetative shoots with densely crowded leaves (in the form of pseudo-rosette) at the apex (Gudžinskas and Žalneravičius 2016). Solidago ×niederederi seemingly originated through multiple events of hybridisation mainly at localities where both parental species grow in proximity. Heterozygosity in ITS regions without signs of recombination or homogenisation confirms its recent hybrid origin (Pliszko and Zalewska- Gałosz 2016; Galkina and Vinogradova 2019). Nilsson (1976), in his open crossing experiment with one plant of S. canadensis and one plant of S. virgaurea, observed that the hybrid progeny originated solely on the latter plant, i.e. in this case S. virgaurea was the maternal plant while S. canadensis served as a pollen donor. Pliszko and Zalewska-Gałosz (2016), based on an analysis of the chloroplast rpl32–trnL locus, stated that hybridisation between S. canadensis and S. virgaurea s.s. can happen in both directions. However, Galkina and Vinogradova (2019) later noticed that both parents are relatively polymorphic at this locus, and therefore it is not possible to clearly determine which of the two species is maternal and which is paternal. Solidago ×niederederi has a limited ability to spread (both vegetatively and generatively) in comparison to the parental species. This is because of the absence of long rhizomes (typical for S. canadensis) and a rather low proportion of well-developed seeds (6%; Migdałek et al. 2014; Pliszko and Kostrakiewicz-Gierałt 2017). On the other hand, the pollen viability of hybrid plants is reduced only slightly (< 70%; Migdałek et al. 2014; Karpavičienė and Radušienė 2016), and the germinability of developed seeds is high (91%; Pliszko and Kostrakiewicz-Gierałt 2017). So far, the spreading of hybrids themselves has not been observed, and the hybrid has not formed its own coherent populations and own geographical range as expected for viable interspecific hybrids. At present, occurrences of S. ×niederederi have been reported from 11 European countries (Jaźwa et al. 2018, but see Results and discussion). Considering the broad overlap of S. canadensis and S. virgaurea s.s. ranges, where hybridisation can be expected, the distribution of S. ×niederederi in Europe seems to be still underestimated (cf. Pliszko et al. 2019).

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 672 Expanding distribution of Solidago ×niederederi in Europe

In this paper, we aim to summarise the known records of S. ×niederederi in Europe and to present its first records in three countries (Slovakia, Hungary, and Romania) within the Carpathian region.

Materials and methods Field surveys, focused on the revision of alien Solidago taxa, were conducted in the Carpathians during 2017–2019 (Czechia, Hungary, Romania, and Slovakia). Altogether, 181 sites of the S. canadensis or S. virgaurea complex were visited; at 17 of these, both species were present. During the survey, several plants of S. ×niederederi were found in the field. They were determined using diagnostic morphological characters identified by Nilsson (1976), Gudžinskas and Žalneravičius (2016), Karpavičienė and Radušienė (2016) and Galkina and Vinogradova (2019). Voucher specimens were deposited in the SAV herbarium (Plant Science and Biodiversity Centre, Slovak Academy of Sciences, Bratislava, Slovakia). To check the distribution of S. ×niederederi in the Carpathian region, the Solidago material from relevant herbaria (BP, BRA, BRNU, PRC, PR, SAV, and SLO) was also studied. The known localities of S. ×niederederi were gathered from literature, herbarium records and observations (i.e. records without vouchers, sometimes documented by photos) from online available databases or webpages (Botanischer Informationsknoten Bayern als Datenportal der Bayernflora 2020; Finnish Biodiversity Information Facility 2020; Forum Flora Austria 2020; Global Biodiversity Information Facility 2020; iNaturalist 2020; Information Facility 2020; Lange and Hermann 2016; Observations du Conservatoire botanique national du Bassin parisien 2020; Smithsonian National Museum of Natural History 2020; SLU Artdatabenken Bruun Asmussen 2020; Sweden’s Virtual Herbarium 2020; Swedish Museum of Natural History 2020; Virtual Herbaria JACQ 2020). In the case of literature or database records which were not documented by herbarium vouchers or photos, their reliability depends on the correctness of taxonomic identification by original authors of these records. Altogether 543 records were gathered: 205 literature records, 151 herbarium records and 187 observations from online available databases or webpages. In the next step, duplicate records from the same locality (136 records) and records from cultivation (3 records) were excluded from further analyses (Supplementary material Table S1). Subsequently, 404 available record data together with 5 new records were used to prepare a distribution map and depict the increasing number of localities in time. To analyse the habitat preferences of the hybrid, available descriptions of habitats in original data were categorised as one of 13 types of habitat: forests, open forest habitats, shrubs and young trees, grasslands, abandoned grasslands, crop fields, abandoned fields, roadsides, quarries, railways, ruderal sites,

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 673 Expanding distribution of Solidago ×niederederi in Europe

Table 1. A list of new distribution records for S. ×niederederi. Number of Co-occurring Locality, date of collection, collector, voucher number(s) hybrid plants Solidago taxa SLOVAKIA, Handlová, close to the dump, roadside; 48.71894°N, 18.7295°E, 592 m a.s.l.; S. canadensis, 2 18 Aug 2018, leg. K. Skokanová (SAV: SOL-N-HAN 1, SOL-N-HAN 2) S. virgaurea SLOVAKIA, Nezbudská Lúčka, valley of Hradský creek, meadow; 49.177339°N, S. canadensis, 18.886282°E, 400 m a.s.l.; 8 Aug 2019, leg. K. Skokanová, P. Mereďa Jr., S. Španiel 1 S. virgaurea (SAV: SOL-N-NEZA 1) SLOVAKIA, Nezbudská Lúčka, site “Za vodou”, roadside; 49.172162°N, 18.879831°E, S. canadensis, 364 m a.s.l.; 8 Aug 2019, leg. K. Skokanová, P. Mereďa Jr., S. Španiel (SAV: SOL-N-NEZB 1, 2 S. virgaurea SOL-N-NEZB 2) S. canadensis, HUNGARY, Abaújvár, slope below the dam, unmanaged grassland; 48.506699°N, 1 S. gigantea, 21.32746°E, 212 m a.s.l.; 29 Aug 2019, leg. K. Skokanová (SAV: SOL-N-ABU 1) S. virgaurea S. canadensis, ROMANIA, Arpaşu de Sus, margin of abandoned field; 45.71156°N, 24.61177°E, 553 m a.s.l.; 1 S. gigantea, 15 Sep 2020, leg. K. Skokanová (SAV: SOL-N-ARP 1) S. virgaurea

dumps, and riparian vegetation (for explanation see Table S1). The information about the number of hybrid plants and co-occurring Solidago taxa were excerpted as well, if available. The distribution map of S. ×niederederi is based on field GPS positioning of 5 new records and coordinates given for 282 previous records (Table S1). For 121 records lacking original geographical coordinates, approximate coordinates were retrieved from Google Earth 7.3.2 (Google Inc.) based on the description of collection sites (100 records) or published maps (22 records; Table S1). A distribution map was prepared using Quantum GIS 3.10 (Open Source Geospatial Foundation). In the paper, we follow the subdivision of Europe into geographic regions according to the United Nations geoscheme (https://unstats.un.org/unsd/ methodology/m49/).

Results and discussion New records of Solidago ×niederederi in the Carpathians Solidago ×niederederi is reported here for the first time from Slovakia (three localities) and Hungary and Romania (one locality each; Table 1, Figures 1, 2). All of them are located within the Carpathians, those from Slovakia and Hungary within the Inner Western Carpathians and those from Romania in the Southern Carpathians. Up to now, the hybrid has been reported within the Carpathians only from the Polish part of the Outer Western Carpathians (cf. Pliszko et al. 2017). The new populations were not individually abundant, as only one or two hybrid plants were recorded at the sites. At all localities, the hybrid grew together with its parental species, and, at two localities, S. gigantea was also present (Table 1). The study of relevant herbarium collections did not reveal any herbarium material of S ×niederederi from Slovakia, Hungary, and Romania, therefore we may assume that it was neglected in the past or that hybridisation between S. canadensis and S. virgaurea s.s. is rather recent and rare in this region due to some reason.

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 674 Expanding distribution of Solidago ×niederederi in Europe

Figure 1. A, B: Comparisons of Solidago ×niederederi from the Handlová (Slovakia) locality (centre) with S. canadensis (left and above) and S. virgaurea (right and below). Solidago ×niederederi in: C: Nezbudská Lúčka, site “Za vodou” (Slovakia), D: Abaújvár (Hungary) and E: Arpaşu de Sus (Romania). Photographs by P. Mereďa Jr. (A, B, C), K. Skokanová (D, E).

General pattern of Solidago ×niederederi distribution in Europe To date, the known occurrence of S. ×niederederi is restricted to Europe. Species of S. virgaurea complex as well as S. canadensis occur also in many regions of Asia (cf. Semple 2020), but, to our knowledge, hybrid taxa between these have not been reported from this area. For more than 50 years, the only record of the hybrid in nature had been one from Austria reported by Khek (1905), until further hybrid plants were recorded in Norway (1955; https://www.gbif.org/occurence/1702356869), France (1956; https://www.gbif.org/occurrence/21592974), and Poland (1957; Rostański 1971). In the following decades, the hybrid also was found in other European countries: Sweden (1966; Nilsson 1976), Denmark (1970; Nilsson 1976), United Kingdom (1979; Burton 1980), Germany (1983; http://id. snsb.info/bfl/collection_bayernflora/31725/1586692), Finland (1990; http://tun. fi/MKC.22152949), and Czechia (1992; https://herbarium.univie.ac.at/database/ detail.php?ID=1165550). The hybrid was recorded at many new sites during the last two decades of the 20th century, mainly in Austria, Germany, and Sweden. Since 2000, the increase in the number of records has continued, with the highest number of new localities reported from Austria (e.g. Pagitz

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 675 Expanding distribution of Solidago ×niederederi in Europe

Figure 2. Distribution of Solidago ×niederederi in Europe. Red stars – new records, yellow circles – records from literature, herbarium collections or observations from online available databases or webpages.

and Lechner-Pagitz 2015; Pliszko et al. 2019), Poland (e.g. Pliszko et al. 2017), and Lithuania (Viltrakytė and Karpavičienė 2014), together with the first/rare records reported from Latvia (Gudžinskas and Petrulaitis 2016), Italy (Pliszko et al. 2019), and the Russian Federation (Vinogradova and Galkina 2019) (Table S1, Figures 3, 4). To sum up, together with the five new records presented here, the hybrid has been reported from 409 sites in 17 countries of the northern, southern (only N Italy), western and eastern European regions. For Finland, France, and Czechia, all records came only from online available databases or webpages (Finnish Biodiversity Information Facility 2020; Observations du Conservatoire botanique national du Bassin parisien 2020; Virtual Herbaria JACQ 2020) (Table S1). The hybrid has been also mentioned in some publications from Finland, France, and Czechia, however without exact localities (Kerguélen 1999; Mlíkovský and Stýblo 2006; Kurtto et al. 2019). All 409 records were restricted to a part of the European continent with temperate (both oceanic and continental) climate conditions between 45.8 and 63.8 degrees of northern latitude (Figure 2). The sites were situated from sea level up to about 1220 m a.s.l. The countries with the highest number of records were Sweden (148), Poland (78), Austria (58), and Germany (47) (Table S1).

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 676 Expanding distribution of Solidago ×niederederi in Europe

Figure 3. Number of records of Solidago ×niederederi in European countries. Red circles – new records, yellow circles – records from literature, herbarium collections or observations from online available databases or webpages. Circle size is directly proportional to the number of localities reported in each country in a particular year (for record details see Table S1). European countries are divided into regions according to the United Nations geoscheme.

According to the data on the abundance of S. ×niederederi (available for 33 from 409 reviewed records; Table S1), usually a single plant has been recorded at a site (20 records). Only in a few cases were two to ten plants reported (ten records), and records with more than ten individuals at one site were very sporadic (three records). Solidago ×niederederi occurs only in areas where S. canadensis and/or S. virgaurea s.s. share their habitats and the abundance of hybrid records reflects (for the most part) the ongoing invasion of S. canadensis. Based on available data for 62 records (from 409 reviewed records; Table S1), the hybrid occurs mainly at sites inhabited by both parental species (58 records) and

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 677 Expanding distribution of Solidago ×niederederi in Europe

Figure 4. Cumulative number of Solidago ×niederederi records in Europe over time (for record details see Table S1).

sporadically at sites inhabited either by S. canadensis (2 records) or S. virgaurea (2 records). The co-occurrence of S. ×niederederi and S. gigantea at a site has been detected only in two new hybrid sites presented in this study and one site in Sweden. The frequency of occurrence of S. gigantea in localities of S. ×niederederi is probably higher, but this information is usually not recorded (e.g., some localities visited in Poland; Skokanová et al. field observations). However, the co-occurrence of S. gigantea should be given more attention, because there is a possibility that the pollen of accompanying related species that are not directly involved in the genome of a hybrid as a parent could help to overcome an interspecific crossing barrier via interaction of heterospecific pollen (Arceo-Gómez and Ashman (2011) and thus contribute to the origin of hybrid individuals. The distribution of S. ×niederederi was repeatedly judged as being underestimated (Pliszko 2013; Gudžinskas and Petrulaitis 2016; Jaźwa et al. 2018; Pliszko et al. 2019). Its unique morphology makes flowering plants of S. ×niederederi relatively easily recognisable even by non-expert botanists in the wild, and confusion with the parental species is not likely. Flowering plants of S. ×niederederi can be confused with S. ×snarskisii. However, the latter differs by having an entirely glabrous stem below the synflorescence and by the presence of rhizomes (Gudžinskas and Žalneravičius 2016). The rather unbalanced geographical coverage of the published records of the hybrid (a dense occurrence in some regions, rare or missing in others) could be affected, apart from the absence of sympatric occurrence of parental species, by the limited accessibility of herbarium and observation data in public databases. However, absence or scarcity of records could be a result of S. ×niederederi being overlooked during field studies, as it often grows in dense patches of S. canadensis and S. virgaurea. The other likely cause is the lack of information in relevant identification keys and national floras.

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 678 Expanding distribution of Solidago ×niederederi in Europe

Figure 5. Habitat preferences of Solidago ×niederederi in Europe based on 268 records with available information on habitat type (for record details see Table S1). European countries are divided into regions according to the United Nations geoscheme.

Habitat and climate Available data on habitat type (in 268 of 409 reviewed records; Table S1, Figure 5) show that the hybrid has been recorded prevalently in abandoned fields (22.7%, 60 records) and other disturbed places influenced by human activities, such as roadsides (17.8%, 48 records), ruderal sites in residential or industrial areas (14.1%, 38 records), quarries (6%, 16 records) and railway habitats (5.2%, 14 records). In the case of forest habitats, S. ×niederederi has been reported mainly in open sites such as forest edges, clearings, or forest roads (11.2%, 30 records). Quite often, the hybrid has been recorded on grasslands, both managed (8.9%, 24 records) and unmanaged/abandoned (5.6%, 15 records). From the survey of available records (Table S1, Figure 5), it is obvious that different types of habitats prevail in particular parts of the distribution area of S. ×niederederi. In northern European countries, S. ×niederederi occurs predominantly on anthropogenic sites, such as roadside, ruderal and railway habitats, dumps, and quarries at low elevations (up to about 160 m a.s.l.), and may be enhanced by the negative impact of human activities. In the Eastern Alps (Austria, Italy) the hybrid grows at elevations of 460–1219 m a.s.l., usually in open forests and shrublands. The recent increase in the number of records of S. ×niederederi in this area (Figure 3) may be attributed to the ongoing spreading of S. canadensis to natural or semi-natural habitats at higher elevations, where it can easily collide with native S. virgaurea s.s. The situation is slightly different in countries of eastern Europe (most data for Poland), where records of S. ×niederederi are restricted to elevations of 60–600 m a.s.l., with abandoned arable fields or grasslands and their margins as the most common habitats. The

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 679 Expanding distribution of Solidago ×niederederi in Europe

exponentially growing number of records of S. ×niederederi during the last decade (2 records before 2010, 104 records after 2010; Figure 3) in some post-Soviet countries and countries that were within the Soviet sphere of influence (Lithuania, Latvia, Poland, Russian Federation) is, for the most part, a consequence of massive spreading of S. canadensis following a strong decline in agriculture after 1989 and persistently absent or perfunctory management of abandoned fields and grasslands (cf. Karpavičienė and Radušienė 2016). This holds also for Slovakia, Hungary, and Romania, from which the first records are reported here. Therefore, it seems likely that the spontaneous hybridisation between S. canadensis and S. virgaurea s.s. will become more common in this part of the Carpathian region in the future. According to Jaźwa et al. (2018), a high probability of hybrid occurrence is expected in areas with an annual temperature range reaching 18–30 °C and minimum temperature of coldest month close to or slightly higher than −10 °C. In addition, the probability of hybrid presence increases with increasing precipitation in the coldest as well as the warmest quarter of the year (Jaźwa et al. 2018). The authors also stated that climatic conditions are the most influential factors determining hybrid establishment and persistence. However, to us, the role of local climatic conditions in shaping the vertical distribution of the parents at the local scale and thus also their local co-occurrence appears crucial. As asynchrony of flowering time is a natural barrier to hybridisation (Bleeker et al. 2007), the mating opportunities of parental species are also dependent on an overlap of their flowering periods which, together with an activity of pollinators, might be influenced by climate conditions at particular sites as well. Therefore, it is important to study how flowering time of S. virgaurea varies in particular parts of its wide range [for example Turesson (1925) observed a month delay in anthesis between lowland, subalpine and alpine ecotypes of this complex] coincides with the flowering time of S. canadensis.

Solidago ×niederederi – genetic pollution as a potential threat to native European flora Fertile plant hybrids that occur sympatrically with their parents often give rise to hybrid swarms and introgressed populations (Preston and Pearman 2015), which can lead to the loss of genetic integrity of native populations (Bleeker et al. 2007). Because S. ×niederederi produces viable pollen (Migdałek et al. 2014), back-crossing with parental species is highly probable. Until now, backcrosses or hybrid swarms of these taxa have not been observed in nature. But a recently detected heterozygosity of ITS sequences in a plant individual that morphologically resembles S. canadensis indicates a probable crossing of S. ×niederederi with the parental species S. canadensis (Galkina and Vinogradova 2019). Therefore, it cannot be ruled out that introgressive hybridisation with S. ×niederederi could cause genetic erosion of native S. virgaurea s.s. (Pliszko and Zalewska-Gałosz 2016).

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 680 Expanding distribution of Solidago ×niederederi in Europe

Moreover, hybridisation of alien plant taxa with native ones can cause the loss of genetic integrity of locally adapted populations such as rare and threatened species (Vilà et al. 2000). It is worth mentioning that in Europe, besides widespread S. virgaurea s.s., other taxa of S. virgaurea complex with more restricted distribution also occur. For example, S. virgaurea subsp. minuta (L.) Arcang. with a patchy distribution in European mountains, and S. virgaurea subsp. pineticola Sennikov, with distribution restricted to the Baltic region, directly occur in areas from which S. ×niederederi is reported. We can assume that potential hybridisation (not recorded yet, but cannot be ruled out for the time being) with S. canadensis could especially threaten the genetic exclusivity and persistence of narrow endemic members of the S. virgaurea complex from sandy coasts of France and Italy – S. litoralis Savi, S. virgaurea subsp. macrorrhiza (Lange) Nyman and S. virgaurea subsp. rupicola (Rouy) Lambinon (Garbari and Cecchi 2000; Tela Botanica 2020). Although the current distribution of S. ×niederederi in Europe is essentially the same as that of S. canadensis, spreading of hybrids themselves is expected, taking into account that fertility of plant hybrids can vary between individuals and later generations are often more fertile than F1s (Preston and Pearman 2015). Moreover, hybrids and further introgressant progeny may be better equipped to thrive in environmental conditions that are beyond the optimum of their parental taxa (Bleeker et al. 2007; Currat et al. 2008; Abbott et al. 2013). The representatives of the S. virgaurea complex are known to have astonishing phenotypic plasticity and a relatively broad environmental niche (Turesson 1925; Takahashi and Matsuki 2016; Hirano et al. 2017; Semple et al. 2020). This in combination with the high invasive potential of S. canadensis could lead to spreading of S. ×niederederi into more natural habitats in future and could pose a threat to native European flora especially in areas of high conservation value such as coastal habitats, subalpine communities, serpentines, dry and mesic grasslands, forest and shrub communities. Therefore, besides monitoring the spread of invasive plants, detailed mapping of the origin, occurrence and behaviour of alien-to-native hybrids is the important precaution to mitigate the negative consequences of plant invasions on native plants.

Acknowledgements We are grateful to curators of the herbaria BP, BRA, BRNU, PRC, PR, SAV, and SLO for allowing us to access their collections. We thank the anonymous reviewers and handling editor Desika Moodley for improving of the manuscript. This study was financially supported by the Scientific Grant Agency VEGA (grant no. 2/0024/19) and by the Slovak Research and Development Agency (grant no. APVV-19-0134).

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Supplementary material The following supplementary material is available for this article: Table S1. Records of Solidago ×niederederi in Europe. This material is available as part of online article from: http://www.reabic.net/journals/bir/2020/Supplements/BIR_2020_Skokanova_etal_SupplementaryMaterial.xlsx

Skokanová et al. (2020), BioInvasions Records 9(4): 670–684, https://doi.org/10.3391/bir.2020.9.4.02 684