Invasive species can be the cause of severe problems for biodiversity, economy and human health. The cup plant (Silphium perfoliatum) is native to eastern North America and is increasingly cultivated in Germany as a new bioenergy crop. Its growth characteristics and autecology do not exclude a possible invasive potential. However, there are hardly any studies on this to date. In this study, habitat requirements for spontaneous colonization and establishment of the cup plant were investigated. Therefore, a 15 m radius around eleven cup plant fields in northern Bavaria (Germany) was examined. Data on cup plant colonization, habitat type, vegetation structure, ground cover, and further site conditions using the Ellenberg indicator values were collected and analyzed by logistic regression models. Spontaneously colonized cup plants were found in a wide range of habitats. Open habitats and human settlement areas were particularly suitable, especially field margins and agricultural paths. A portion of open soil of about 25% was preferentially colonized. Cup plants occurred predominantly within the first few meters of the field margin and increasingly around cup plant fields that have existed for a longer period. Favorable for the development of stems and thus for flowering, fruiting and establishing are warmer sites with a high herb layer. Individual plants that had developed a stem persist for several years and increased their stem number over time. The number of stem-developing individuals also increased over time. Thus, there exist an enormous potential for spread in the future. However, an invasive potential could not be confirmed based on the present study, because a threat of biodiversity was not proven.

alien, bioenergy crop, casual occurrences, dispersal distance, distribution, establishment, habitat requirements, invasive potential

An increasing number of plant species are being introduced by humans into regions where they do not occur naturally (Seebens et al. 2017). Some of these plants can settle permanently within these new areas, often at ruderal sites but also in natural and semi-natural habitats (Kowarik and Rabitsch 2010). A few become invasive and cause severe problems for biodiversity, economy and human health (Vitousek et al. 1996; Andersen et al. 2004; Kowarik and Rabitsch 2010). Some of these species were introduced unintentionally, and others intentionally e.g. as crops. The example of the Jerusalem artichoke (Helianthus tuberosum) shows that large-scale cultivation of plants without previous investigation of potential invasiveness can be fatal. This species is firmly established in many European countries and is partly responsible for soil erosion and suppression of native vegetation in the floodplains of rivers (Kowarik and Rabitsch 2010). Another introduced crop that has increasingly been cultivated in Germany in recent years is the cup plant (Silphium perfoliatum). So far, there are hardly any studies on the possible invasiveness of this species. The cup plant was introduced to Germany in 1762 as an ornamental plant (Brennenstuhl 2010). Since 2004 it has been cultivated as a bioenergy crop (Frölich et al. 2016). Good yields, low effort after establishment and many ecological advantages compared to the predominantly cultivated biogas crop maize (Zea mays) are reasons for increasing cultivated cup plant fields (Frölich et al. 2016). In 2021, the cup plant was cultivated on around 10,000 ha of arable land in Germany, nearly tripling the area in one year (FNR 2022).

The cup plant is a perennial, yellow-flowering hemicryptophyte of the Asteraceae family and is native to the prairies of eastern North America (Stanford 1990; Jäger 2017). It grows 2–4 m high and can develop several hundred flower heads, each with 20–30 fruits (Stanford 1990; Dauber et al. 2016; Ende et al. 2021). The flowering period is from July on, fruits ripen from August onwards and then drop out (Jabłoński and Kołtowski 2005; Penskar and Crispin 2010; Wrobel et al. 2013; Jäger 2017). Seeds have a physiological dormancy, which can be broken by low or alternating temperatures, so that germination under Central European climate is possible (Gansberger et al. 2017). The high productivity and high reproductive potential of cup plant could lead to invasiveness, in case of spontaneous spread into sensitive habitats that are relevant for nature conservation. Following EU legislation, a species is being classified as invasive if its spread threatens biodiversity (Article 3 No. 2 EU-Regulation No. 1 143/2014). The Netherlands and Russia already classify the cup plant as potentially invasive (Matthews et al. 2015; Vinogradova et al. 2015). Detections of spontaneous occurrences of cup plants have been made in several European countries and for 15 of Germany’s 16 federal states (Roskov et al. 2019; GBIF 2021). However, knowledge of dispersal distance and requirements on soil, vegetation or habitat for spontaneous colonization is low. Therefore, we investigated an area within a 15 meter radius around eleven cup plant fields in northern Bavaria (Germany) and collected data on cup plant occurrence in combination with habitat type, vegetation structure, ground cover, and other site conditions using the Ellenberg indicator values (Ellenberg and Leuschner 2010). We asked the following questions: What are the crucial site conditions that enable a spontaneous colonization of cup plants and subsequently their establishment? How do establishing (stem-developing) individuals develop over three years? Spontaneous colonization and establishment in habitats that are relevant for nature conservation would be more problematic for biodiversity than, for example, in ruderal sites or roadsides (Nehring et al. 2015). Our study is limited to northern Bavaria over three years. Nevertheless, the results provide important insights into the habitat requirements and development of cup plant that are valid beyond this small region and are essential for assessing the possible invasiveness of cup plant.

The present study is the first one which comprehensively investigates habitat requirements of the cup plant for spontaneous colonization and establishment in Germany. Results showed that cup plants were able to invade a wide range of habitats and were found around all of the eleven investigated fields in northern Bavaria.

One of the most crucial parameters for spontaneous cup plant occurrence was the distance to the cup plant field. On average, cup plants were spread at distances of only 2.1 m, and there was a strongly negative relationship between cup plant occurrence and distance to the field (Fig. 1B). Fruits as well as root parts if they contain buds can serve as diaspores (Stanford 1990; Czarapata 2005). Dispersal of root parts would presuppose a cutting or damage of roots which could happen e.g. when ploughing. Because all of the investigated fields were not ploughed since cup plant is cultivated there, we assume that all of the detected spontaneously settled cup plants are developed from seeds. The vectors for the dispersal of cup plant fruits have not been well investigated so far. According to Jäger (2017), fruits are dispersed by shaking of fruiting stems which fits in with the low dispersal distances in the present study. However, single individuals were still found up to 14 m distant to the field, which nearly corresponds to the limit of investigated radius of 15 m. This dispersal distance cannot be achieved by shaking. Hence, there must be another dispersal vector. The fruits of cup plant are equipped with two tiny wings that could enable them to fly (Kowalski and Wierciński 2004) and thus be carried over longer distances. Nevertheless, wind dispersal seems not to play a major role, because most of the cup plants were detected in the immediate vicinity of the fields. Ende and Lauerer (2020) documented a spread of cup plants of up to 700 m along a street and presumed agricultural machines as vector. In fact, losing of crop and thus of fruits from the trailer is quite possible and must be kept in mind regarding the prevention of cup plant spread. A dispersal of the fruits and of root parts via water would also be conceivable and was suspected by Ende et al. (2021) and Vladimirov (2021). Altogether, we suspect a certain dispersal potential of cup plant – even over longer distances.

The probability of spontaneous cup plant occurrence increased almost linearly with increasing field age (Fig. 1C). This is not surprising, because the spontaneously colonized cup plants are perennial and can persist over many years (Stanford 1990). Every year, plants can be added and accumulate to an increasing number with increasing field age. Cup plant fields are usually used for 10 to 15 years, sometimes even longer (Dauber et al. 2016; Frölich et al. 2016; Hartmann and Lunenberg 2016; Bernas et al. 2021). The fields investigated in our study were between 2 and 11 years old. A further increase in spontaneous colonization can be expected in the coming years. Together with the continuously increasing area that is cultivated with the cup plant (FNR 2022), this results in an enormous spreading potential for the future emanating from the fields throughout Germany.

Another important parameter for the spontaneous colonization of cup plants seems to be the portion of open soil. In our study, cup plants occurred preferentially on about 25% open soil (Fig. 1D). It is a matter of speculation why just this value is optimal for colonization. A lower portion of open soil goes along with a higher cover of vegetation, of paved ground, or of litter. However, none of these parameters was significantly decisive for cup plant occurrence. Notwithstanding this, these three factors could still impede germination and/or seedling development. It is known that cup plant seedlings develop slowly and are therefore very sensitive to competing vegetation in the first year (Köhler and Biertümpfel 2016). In the present study, a high portion of open soil was mainly found on unpaved paths and occasionally under dense scrubs or hedges. Colonization is more difficult on paths due to strong soil compaction and under woody formations due to lower light availability. Stanford (1990) confirms that cup plants need full sun for optimal growth.

All other parameters (besides habitat type), i.e. Ellenberg indicator values (EIV) for soil reaction, light availability and soil moisture, cover of litter, of shrub and of tree layer, as well as the cover of paved ground, did not influence the probability of cup plant occurrence.

In the first year of growth, cup plants develop only a rosette of leaves. From the second year on it can develop stems, flowers, and respectively fruits (Wrobel et al. 2013). These stem-developing individuals were considered as establishing in the present study. Such establishing individuals were also found around each of the eleven surveyed fields. More than half of the plots that were colonized by cup plants also had establishing individuals (59%). A flower development could not be assessed because the cup plant blooms between July and October in Central Europe (Jabłoński and Kołtowski 2005; Wrobel et al. 2013; Jäger 2017) and data were collected between May and early August. However, most of these individuals had only one stem, were not very tall and less vigorous than the cultivated cup plants on the field. We therefore assume that most of these plants could only develop a few flowerheads at most.

In the study area the following habitat types were represented: open habitats, human settlement areas, woody habitats, and inland waters including their riparian areas. However, cup plant did not invade these habitat types equally (Fig. 1A). The habitat type had a significant impact on the probability of cup plant occurrence. Cup plants preferred open habitats such as field margins and human settlement areas especially paths, but also occurred spontaneously in intensively used grasslands. All these habitat types are cut regularly, so that successful fruit development and further spread are unlikely. This is reflected in the significantly positive relationship between the probability of cup plant establishing and the height of the herb layer in the present study (Fig. 2C). Due to the nutrient-rich and species-poor characteristic of the mentioned habitat types their value for biodiversity is quite low. Hence, an invasion of cup plant is initially unproblematic here. Open habitats without management were hardly represented in our study. However, cup plant occurrences in ruderal and fallow areas are frequently detected in Germany (Buhr and Kummer 2009; Brennenstuhl 2010; Nezadal et al. 2011; Schönfelder 2012; Klug 2015; Parolly and Rohwer 2016; Jäger 2017; Kämpfe 2017). There a successful fruit development and further spread is conceivable.

In the present study, the cup plant also invaded woody habitats, although the probability of its occurrence was only about one third as high as in open habitats. The herb layer of woody habitats is usually not managed, which is why reproduction and further spread of cup plant is potentially possible. However, an extensive spread in forests or plantations is not expected, because cup plant needs full sun for optimal growth (Stanford 1990). Additionally, the probability of establishing grew with increasing EIV temperature in the present study (Fig. 2A). The cup plant therefore prefers warmer sites for stem development than it needs for rosette stage. Stanford (1990) confirms that cup plants develop best at around 20 °C. In fact, only three of the cup plants that invaded forests and plantations, have developed stems. In tree rows and tree groups stem development succeeded more often because the required light, warmth and absent management is available there. Less management could also be the reason for the positive relationship between the probability of cup plant establishing and distance to the field (Fig. 2B). In contrast to the general occurrence of cup plant, its establishing increased with the distance to the field. Usually, the habitats in the immediate field vicinity are intensively mowed and managed, which prevents stem development. Habitats farther away from the fields may be more heterogeneously structured, which is why stem development may succeed more often. In literature, there is little evidence of spontaneous detections of cup plants in woody habitats. Only Reuther and Tillich (1996) detected it in a scrub fringe in Germany. In its native range in eastern North America, it colonizes amongst others in woods, thickets and roadside ditches (Penskar and Crispin 2010). However, cup plants preferentially colonize there near rivers: in open prairie clearings in moist sandy bottomlands, in lakesides, and in ravines (Stanford 1990; Penskar and Crispin 2010; Gansberger et al. 2015). In Germany, too, the cup plant was frequently found in the riparian areas of standing and running water (Oberdorfer 1994; Brandes 2003; Wölfel 2013; Parolly and Rohwer 2016; Jäger 2017; Schönfelder 2017). In the present study, inland waters including their riparian area were not invaded. However, this habitat type was hardly represented in our study. Furthermore, not even a significant relationship between EIV soil moisture and cup plant occurrence or establishing could be proven in the present study. This was possibly because all the investigated sites had an average EIV soil moisture. But the preference of cup plants for moist sites was also confirmed by experimental studies in Germany by Ende et al. (2021), where it showed higher biomass and reproductive potential under moist soil conditions. Therefore, special attention must be paid to moist habitats because they are often valuable for nature conservation and could be colonized by the cup plant (Ende et al. 2021). In our study, other valuable ecosystems were also hardly represented. Only two sites fall into this category: A pine forest on a nutrient-poor, base-deficient site where one single spontaneously colonized cup plant in rosette stage occurred and a species-rich, extensively used grassland where no cup plant occurred. According to literature, no spontaneously colonized cup plants have been detected in valuable ecosystems in Germany so far. However, future colonization cannot be excluded.

Once a spontaneously colonized cup plant has developed stems, the question arises whether and how they develop over time. Our results showed that all of the monitored establishing cup plants survived and new ones were added over the observational period of three years. The number of establishing individuals increased six-fold within these three years. The number of stems per plant increased over this time. Boe et al. (2019) also observed that the cup plant develops more stems with increasing age. All these individuals might develop flowers and eventually reproduce. Therefore, the reproductive potential increases over time both per plant and per population. The factor time is therefore of great importance for assessing the invasive potential of the cup plant.

The present study demonstrated an enormous spreading potential of the cup plant. Regarding the future, spontaneous occurrences are likely to expand as the number of cup plant fields increases. The cup plant is able to colonize and establish in a wide range of habitats, especially in less managed open habitats with disturbances. An invasive behavior has not yet been detected. However, there are still some unanswered questions regarding its possible invasiveness. Further studies, especially on dispersal vectors and competitive strength, as well as further documentation of spontaneous occurrences, are necessary to assess the risk of the continuing spread of cup plants and its impact on the native flora and fauna. Until further knowledge is available, we recommend cautious handling of the cup plant. Fields should be located at a safe distance to valuable ecosystems and watercourses to avoid possible dispersal of diaspores via water and an invasion of these ecosystems. Agricultural machines should be cleaned thoroughly after use and covered before leaving the field to prevent dispersal of fruits over long distances.

We thank the Oberfrankenstiftung and the District Government of Upper Franconia subject area water management for financial support as well as the Studienstiftung des deutschen Volkes for scholarship of the first author. The APCs were funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – 491183248 and the Open Access Publishing Fund of the University of Bayreuth. Special thanks are given to the farmers of the cup plant fields for their support and advice. Anna Walentowitz is thanked for proof reading.