Annual weedy species of Erigeron in the northern Iberian Peninsula: a review

. A revision of the alien Erigeron species formerly included in Conyza found in the northern Iberian Peninsula is presented. A close examination of numerous specimens collected by the authors as well as voucher specimens preserved at several herbaria has helped to clarify several aspects regarding this group. Four species have been recognised in the study area: Erigeron canadensis (= Conyza canadensis ), E. bonariensis (= C. bonariensis ), E. sumatrensis (= C. sumatrensis ) and E. floribundus (= C. floribunda , including C. bilbaoana ). They occupy anthropogenic habitats, such as road edges, abandoned fields, crops and waste ground, as well as natural and semi-natural communities, such as nitrophilous river bar communities and ruderal communities on coastal dunes subjected to substantial levels of anthropogenic disturbance. Erigeron sumatrensis and E. floribundus emerge as the two most frequent taxa. Erigeron canadensis , regarded in the past as the most widespread species of the group, is almost absent from the study area, especially from the Atlantic watershed. Furthermore, an important number of specimens previously identified as E. bonariensis do actually correspond to E. sumatrensis . No hybrids have been found. A detailed identification key highlighting the main features that help to separate the four Erigeron species is presented. Finally, as E. floribundus is the most controversial species in the group and the last to arrive, we include a study of its expansion across western Europe, where it has become a frequent alien especially along the Atlantic regions in the last century.


Introduction
Erigeron L. (Asteraceae) is a taxonomically complex genus which comprises at least 400 annual, biennial and perennial species, mostly in temperate regions (Nesom, 2006). This genus and the genus Conyza Less. have been traditionally considered as two separate but closely related genera [e.g. Stace 2010 in the 3 rd edition of the New flora of the British Isles and Benedí et al. (2019) in Flora Iberica], although their distinction has long been problematic (Nesom, 1990(Nesom, , 1994. However, it has been shown that Conyza is polyphyletic and nested within Erigeron (Noyes, 2000) and, thus, some authors merge Conyza into a widely delimited genus Erigeron. This wide concept of Erigeron that includes species formerly included in Conyza is commonly accepted [e.g. Greuter (2003) in the Euro+Med treatment of Astereae, Tison & de Foucault (2014) in Flora Gallica and Stace (2019) in the 4 th edition of the New Flora of the British Isles].
Forty-five species of Erigeron are present in Europe and the Mediterranean basin according to Euro+Med PlantBase (Euro+Med, 2006-2020. They include a number of taxa formerly included in Conyza that have been introduced in the last decades and centuries into Europe and the Mediterranean basin (Euro+Med, 2006-2020, where they occur mainly in disturbed habitats, such as wasteland, abandoned fields, cultivated ground, roadsides or railways, although they can also be found in natural and semi-natural habitats such as sand dunes or grasslands (Thébaud & Abbott, 1995;Mundell, 2001;Campos et al., 2004;Campos, 2010). Among these, the most widespread ones are E. canadensis (=C. canadensis), E. bonariensis (=C. bonariensis), E. sumatrensis (=C. sumatrensis) and E. floribundus (C. floribunda, including C. bilbaoana) (Mundell, 2016; see Table 1 for authorities). Additionally, despite Erigeron invasive species having very low hybridogenic activity (Galkina & Vinogradona, 2020), hybrids between E. canadensis and E. bonariensis (Wurzell, 1994;Mundell, 2016) and between native E. acris and E. canadensis, as well as between E. sumatrensis and E. floribundus have been reported from the UK and Ireland Mundell, 2016). It is also worth mentioning several hybrids described at the beginning of the 20 th century in the NE Iberian Peninsula by Frère Sennen, such as those between E. canadensis and Conyza ambigua (=C. x flahaultiana), E. canadensis and C. naudini (C. x rouyana), C. naudini and C. ambigua (C. x daveauana), C. naudini and E. coronopifolium (E. x mixtum) and E. coronopifolium and C. ambigua (E. x barcinonense) (Sennen 1908(Sennen , 1917.

ARTICLES
Erigeron canadensis is thought to be native to North America (Cronquist, 1976) and was introduced into Europe at the beginning of the 17 th century (Marshall & McClintock, 1972;Prieur-Richard et al., 2000). It is a highly successful invader which is now widely spread across the globe. Regarding E. bonariensis, this species is native to South America and it was first recorded in Europe in the 18 th century (Prieur-Richard et al., 2000), where it has naturalised especially across the Mediterranean basin and Atlantic regions of SW Europe (Milović, 2004) given its more thermophilous requirements (Wurzell, 1988(Wurzell, , 1994Zambrano-Navea, 2013). However, it can also occur, with lower abundance, in northern countries such as the UK (Wurzell, 1988;Rand, 2008), Belgium (Verloove & Boullet, 2001;Verloove, 2006) or Norway (Gederaas et al., 2012). With respect to E. sumatrensis, this species is native to South America as well, although it was first named from Sumatra where it is an alien (McClintock & Marshall, 1988;Mundell, 2001). It was introduced into Europe, namely France, during the 19 th century (Thébaud et al., 1996). At the beginning of the 20 th century it was already expanding across France, Spain and Portugal (Milović, 2004) and in 1984 it was recorded for the first time in Great Britain (Wurzell, 1988), though it had already been reported from the Channel Islands in 1961 (Jee, 1962;Stace & Crawley, 2015). As Milović (2004) pointed out, this species has been widely confused with E. bonariensis as a result of their morphological and ecological resemblance and the lack of an appropriate literature (see for example comments in Wurzell, 1988Wurzell, , 1994. According to Thébaud & Abbott (1995), E. sumatrensis, along with E. canadensis, is probably among the most widespread species found throughout the world. Finally, E. floribundus arrived in SW Europe at the beginning of the 20 th century and has been spreading since then. However, Verloove & Sánchez Gullón (2008) mentioned that this species has been surprisingly overlooked in Spain by some authors such as Campos & Herrera (1997) and Sanz-Elorza et al. (2004), with just a few references from northern regions (Aedo et al., 2001;Verloove & Sánchez Gullón, 2008).
The paucity of references for this species in Spain may reflect the treatment of the genus in regional floras of this country. Aizpuru et al. (1999) did not include E. floribundus (either as C. bilbaoana or C. floribunda) in their illustrated keys to the flora of the Basque Country and neighbouring territories, given that it was not known to be present in the territory covered by the flora. In the same way, Bolòs & Vigo (1996) neither took E. floribundus into account in their flora of Catalonia and neighbouring regions, but did consider another species named Conyza blakei (Cabrera) Cabrera. However, Laínz (2002) stated that the description of C. blakei given in the Catalan flora did not match the description on the flora of Buenos Aires province (Cabrera, 1963(Cabrera, -1970 and that accordingly C. blakei sensu Bolòs & Vigo (1996) was in fact C. bilbaoana (=E. floribundus) (González-Martínez, 2015). In any case, genuine C. blakei is present in SW France (Tison & de Foucault, 2014), and it might also be scattered across northeast Spain (Bolòs & Vigo, 1996). Its present (or future) occurrence in the Basque Country and neighbouring territories cannot be ruled out (F. Verloove, pers. comm.). Additionally, and adding more to this confusion, Flora iberica, which constitutes the reference work for vascular plants of the Iberian Peninsula and the Balearic Islands, has recently released a volume covering part of the Compositae family (Benedí et al., 2019) in which Conyza and Erigeron are treated as two separate genera and, more importantly, where Conyza canadensis and C. bonariensis are accepted as the only alien Conyza species present in this territory (Morales, 2019).
Hence, in the Iberian Peninsula important doubts have long existed regarding the identification of numerous annual weedy Erigeron specimens, especially those glabrescent plants that did not match the wellknown E. canadensis. Therefore, in the present work we have examined specimens collected in the northern Iberian Peninsula in order to (1) determine which species of annual weedy Erigeron are currently present; (2) develop a detailed identification key highlighting the main features that help to separate the different annual weedy Erigeron species distinguished in the study Table 1. Synonyms for the different Erigeron (formerly Conyza) species identified in the northern Iberian Peninsula.
Nomenclature followed indicated in bold.
area; and (3) estimate which species are more frequent. Additionally, we present a study of the expansion of E. floribundus in western Europe as this is the most controversial taxon of the group.

Methods
The study area for the present work corresponds to the regions of Cantabria, Basque Country, Navarre and neighbouring territories in northern Spain. This area is drained by two watersheds separated by the Cantabrian Mountain Range: Atlantic on the north, with streams flowing into the Bay of Biscay, and Mediterranean on the south, with streams flowing into the Ebro River ( Figure 1). Within this area, the vast majority of the specimens were collected between Cantabria in the west and northern Navarre in the east. Initially, we focused on specimens collected by the authors and other members of the Flora and Vegetation Research Group of the University of the Basque Country (UPV/EHU) along with voucher specimens preserved at the BIO herbarium of the same institution. Subsequently, in order to study as many Erigeron specimens from the study area as possible, we also examined voucher specimens sent on loan by the following herbaria: ARAN (Aranzadi Society of Sciences), SEST (Natural Sciences Society of Sestao) and VIT (Natural History Museum of Álava). These herbaria also contained voucher specimens from SW France (Atlantic Pyrenees department) that were also examined (Appendix S1). A total of 261 voucher specimens were studied. To characterise morphologically the different annual weedy Erigeron species found in the study area, the following vegetative and reproductive traits were measured: leaf length, leaf width, stem hairs length, capitula length and width, number of tubular and ligulate florets per capitulum, number of lobes per tubular floret, and ligule length of ligulate florets. Additionally, the original descriptions of the taxa involved were consulted.
Distribution maps for the northern Iberian Peninsula based on the examined specimens are presented. For this purpose, bibliographical references were not considered since we cannot confirm whether the identification fit the criteria included in the aforementioned key. Information on the examined specimens regarding province, locality, 1x1 km UTM grid square (ED50 datum), site description, elevation, date and authors of collection and registration code in the corresponding herbarium is shown in Appendix S1.
Finally, a map showing the distribution and earliest records of E. floribundus in western Europe was created in order to analyse its geographical expansion in this territory. For this purpose, bibliographical references and own unpublished data were used along with occurrences provided by the following electronic resources: Global Biodiversity Information Facility (GBIF, worldwide; https://www.gbif.org), Inventaire National du Patrimoine Naturel (INPN, France; https://inpn.mnhn. fr), National Biodiversity Network Atlas (NBN Atlas, UK; https://records.nbnatlas.org), the Botanical Society of Britain and Ireland (BSBI, UK and Ireland; https:// bsbi.org/maps) and the Plant Information System of Spain (ANTHOS, https://www.anthos.es). These results are presented in 50 x 50 km grid cells.

Results and Discussion
Annual weedy Erigeron species in the northern Iberian Peninsula and identification key for their distinction Four annual weedy Erigeron species formerly included in Conyza have been identified in the northern Iberian Peninsula: E. canadensis, E. bonariensis, E. sumatrensis and E. floribundus (Figure 2; see Table 1 for synonyms). This result is in line with what has been reported from other European countries (e.g. Mundell, 2016;Verloove, 2019). However, as already commented above, Flora Iberica only considers E. canadensis (sub Conyza canadensis) and E. bonariensis (sub Conyza bonariensis) to be present in the Iberian Peninsula, in line with the treatment of Conyza in Flora Europaea (Cronquist, 1976). Our findings, though, clearly overcome this outdated genus outline, in agreement with the trends observed in the last decades across Europe, where some additional Conyza species have been recognized and accepted (Verloove, 2006;Rand, 2008;Mundell, 2016), sometimes with a varying nomenclature. Of these, C. sumatrensis and C. floribunda (many times as C. bilbaoana) are clearly amongst the most widespread ones and have been erroneously included in Flora iberica within C. bonariensis (Morales, 2019). With respect to C. sumatrensis, according to Morales (2019), this species could not be recognised in the territory covered by Flora iberica on the basis of the diagnostic characteristics included in the literature consulted by the author. Additionally, Morales (2019) also argues that the great morphological variability of C. bonariensis implies that a number of taxa have been described and that some forms of this species had been identified as C. sumatrensis. In our opinion, though, they are clearly distinct taxa that can be distinguished on the basis of both morphological features, such as plant height and robustness, width of stem leaves, inflorescence shape, capitula width, number of tubular florets per capitulum and colour of the apex of the involucral bracts (see key below), and genetic features (Thébaud & Abbott, 1995;Galkina & Vinogradova, 2020). In the same way, regarding C. floribunda, this species can be also clearly distinguished from C. bonariensis both morphologically (e.g. stem and leaves hairiness, inflorescence shape, number of tubular florets per capitulum, capitula width and involucral bracts hairiness) and genetically (Thébaud & Abbott, 1995).
Summarising, we are in disagreement with Flora iberica over the approach on Conyza and we propose that at least four species of Conyza can be found in the northern Iberian Peninsula (C. canadensis, C. bonariensis, C. sumatrensis and C. floribunda). This implies that C. sumatrensis and C. floribunda should be regarded as separate taxa that can be clearly distinguished from C. bonariensis. Furthermore, these Conyza species should be included within Erigeron (Greuter, 2003;Stace, 2019;Verloove, 2019).
Below we provide an identification key for mature individuals of these alien Erigeron species based on own observations and measurements made by the authors in a number of Erigeron specimens and previous works (Campos, 2010). It is worth highlighting the differences in the inner involucral bracts between E. floribundus and E. canadensis, which have not been pointed out in previous keys (but see Mundell, 2001). We consider that this feature could allow a quick and robust separation of these taxa. Regarding glabrescent taxa, E. canadensis was previously thought to be much more common than E. floribundus across the study area. As a matter of fact, it was listed among the 50 most frequent alien species in the Basque Country across a wide range of habitats, being E. floribundus absent from this list (Campos et al., 2013). However, a close examination of numerous glabrescent specimens pointed out that almost half of the voucher specimens previously identified as E. canadensis were in fact E. floribundus (Table 2), many of them from the Atlantic watershed. This suggests that E. floribundus is actually the species that is widely spread across this region (Figure 3), which is in accordance with previous research suggesting that C. bilbaoana (=E. floribundus) is probably the commonest representative of the genus in SW France and that it has been surprisingly overlooked in Spain (Verloove & Sánchez Gullón, 2008). Additionally, and according to several voucher specimens examined, E. floribundus would have been present in inland and coastal localities of the study area since at least the early 1980s. E. canadensis, on the other hand, would be almost absent from the Atlantic watershed since only a few specimens collected in the 80s and 90s in the Basque Country and SW France, respectively, were confirmed as such. This misidentification has also been reported from another oceanic territory such as New Zealand, where true Conyza canadensis (=E. canadensis) is a rare plant and it is the widespread C. bilbaoana (=E. floribundus) which is known there as 'Canadian fleabane' due to an early identification error (Kent, 1991;Stanley, 1996;Mundell, 2001). In the words of Kent (1991), in New Zealand C. canadensis would be 'part of a complex, the true species being rare, and the most widespread being the South American C. bilbaoana'.
Conyza albida x bonariensis --1 1 -- With respect to the pubescent taxa, our examination revealed that a significant number of specimens previously identified as E. bonariensis were in fact E. sumatrensis (Table 2). A possible explanation for this is that, as previously mentioned, the regional key in Aizpuru et al. (1999) does not include E. sumatrensis and considers E. bonariensis as the only pubescent taxon of the genus. This regional key does include Conyza albida (a synonym for E. sumatrensis), but the description matches partly that of E. floribundus. This, along with the great amount of E. sumatrensis recently recorded in the study area (Figure 3), suggests that this species is much more frequent than E. bonariensis, which is in accordance with previous works (e.g. Campos, 2010).
No hybrids have been found among the specimens that have been examined in the framework of the present study.

Expansion of Erigeron floribundus in western Europe
Erigeron floribundus is the most controversial taxon in the group of Erigeron species formerly included in Conyza. As previously discussed, its resemblance to other similar species, especially E. canadensis, caused that it was usually overlooked in many regions and countries. Figure 4 shows the distribution and expansion of E. floribundus in western Europe in the last century.
According to the Global Biodiversity Information Facility (GBIF) and the French Inventaire National du Patrimoine Naturel (INPN), E. floribundus was first recorded in the early 20 th century in Marseille (1903) and nearby Toulon (1912) in southeast France, which would constitute the first records for this species in Europe ( Figure 4). However, caution should be taken since several records originally identified as Erigeron naudini, a synonym for E. sumatrensis (Wurzell, 1988), reported from the first half of the 20 th century in southeast France, have been included in GBIF as E. floribundus. Although it is found in central and south-eastern France, especially in the Occitanie region, its main distribution range in this country encompasses the Atlantic regions, where it can achieve high abundances. In southwest France it is known since the early 1960s from Anglet (Aedo et al., 2001)   in the study area based on the examined voucher specimens (see Appendix S1).
In Spain, E. floribundus has been present since at least the 1980s in the Bay of Biscay and the Ebro basin in the north of the country, although a 1963 citation without voucher specimen from Hondarribia near the French border (Aedo et al., 2001) could mean that this species has been present in this territory since long before ( Figure 4). It is especially abundant in the Bilbao metropolitan area. In the Galicia region (NW Spain) E. floribundus is known since 1966 (Aedo et al., 2001), though most of the references for this region are much more recent. It has also been recorded from Extremadura and Andalusia regions in southwest Spain, where it has been present since at least 1993. In nearby Portugal, few references of E. floribundus are available so far. It was first recorded (as Conyza bilbaoana) in 2004 from Vila Nova de Gaia in the north-western part of the country and regarded as a new neophyte to the Portuguese flora (Alves & Aguiar, 2012). However, according to GBIF there are two references from 1970 in southeast Portugal near the south-western Spanish records, meaning that this species could have been present in Portugal and the south-western Iberian Peninsula since long before.
Erigeron floribundus has also reached the UK and Ireland where it has become a widespread alien in some areas. In the UK it was not recognised until 1994, when a population of a robust Conyza species collected in Southampton (S England) in 1992 and clearly different from C. canadensis was identified as C. bilbaoana (Stanley, 1996). Subsequently, a record from 1977 in Essex (SE England) (Stace & Crawley, 2015) and a 1974 specimen from Flintshire in northern Wales (Hipkin et al., 2012) were uncovered. It has also been found in Scotland, where it was first collected in Fochabers in 2005, and Northern Ireland where, according to the Botanical Society of Britain and Ireland (BSBI), it was first recorded from Belfast in the 2000s ( Figure  4). E. floribundus is especially frequent in Greater London, southern England between Bournemouth and Portsmouth and southern Wales where, according to the National Biodiversity Network Atlas, it is known from Swansea since 2001. It has probably arrived in the UK from Brittany (Stace & Crawley, 2015). Similar to what has been described for the UK, E. floribundus was first recognised in Ireland in 1996 when a population found near New Ross (SE Ireland) in 1992 was identified as Conyza bilbaoana (Reynolds, 1997). However, specimens of this species had been previously collected in Dublin in 1984 and 1985, although they were not identified as such until 1996 (Reynolds, 1997;Mundell, 2016). Subsequently, it was found in other parts of the country, such as the south-western coast, where it is known from Tralee since 1995 (Reynolds, 1997) and the north-western coast, where it was first detected in the 2010s. According to BSBI, it is nowadays a frequent alien in the Dublin area and the south-eastern coast between Waterford and Wexford. Finally, E. floribundus has also been found in Belgium and the Netherlands. Regarding Belgium, it was first collected in 1999 in the Kortrijk area (Verloove, 2001). Subsequently, it has been found across the country, especially Flanders, with a concentration of records in the south of West-Flanders where the first populations were detected and having also spread to the rest of the region, except for the Polders and Kempen areas (F. Verloove, pers. comm.). It is also known from Brussels and, in recent years, it has been found in Wallonia, where it is still scarce. In relation to the Netherlands, it was first found in the early 2000s in Rotterdam and has since then been detected in other parts of the country (Figure 4). It is precisely in Rotterdam and surrounding areas where more records of E. floribundus are available.

Conclusions
Four annual weedy species of Erigeron formerly included in Conyza have been identified in northern Spain: E. canadensis, E. bonariensis, E. sumatrensis and E. floribundus. All of them occur mainly in anthropogenic habitats, although they can also invade natural and semi-natural communities, such as nitrophilous river bar communities and ruderal communities on coastal dunes. Erigeron floribundus and E. sumatrensis are the most widespread taxa of this group in the northern Iberian Peninsula. Erigeron canadensis, regarded in the past as the most widespread taxon in this region, is almost absent nowadays, especially from the Atlantic watershed.
Erigeron floribundus has spread across western Europe in the last decades, especially along the Atlantic regions, although it can also be found in Mediterranean localities. The history of its expansion is discussed, from the initial (though uncertain) references from southeast France in the early 20 th century to the most recent detections in Belgium and the Netherlands. The pattern of detection of E. floribundus in western Europe suggests that this species could have been introduced independently at different times in different locations.